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Systematics of the Neotropical Genus Leptodactylus Fitzinger, 1826 (Anura:Leptodactylidae): Phylogeny, the Relevance of Non-molecular Evidence, andSpecies AccountsAuthor(s): Rafael O. de Sá, Taran Grant, Arley Camargo, W. Ronald Heyer, Maria L. Ponssa, EdwardStanleySource: South American Journal of Herpetology, 9():S1-S100. 2014.Published By: Brazilian Society of HerpetologyDOI: http://dx.doi.org/10.2994/SAJH-D-13-00022.1URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-13-00022.1

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Systematics of the Neotropical Genus Leptodactylus

Fitzinger, 1826 (Anura: Leptodactylidae): Phylogeny, the

Relevance of Non-molecular Evidence, and Species Accounts

Rafael O. de Sá1,*, Taran Grant2, Arley Camargo1,3, W. Ronald Heyer4, Maria L. Ponssa5, Edward Stanley1,6

1 Department of Biology, University of Richmond, Richmond, Virginia, 23173, USA.2 Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, CEP 05508-090, São Paulo, SP, Brazil. Email: [email protected] Current Address: Centro Universitario de Rivera, Universidad de la República, Rivera 40000, Uruguay. Email: [email protected] Department of Vertebrate Zoology, Smithsonian Institution, Washington, DC 20560, USA. Email: [email protected] Fundación Miguel Lillo, San Miguel de Tucumán, Tucumán, Argentina. Email: [email protected] Herpetology, California Academy of Sciences, Herpetology, California Academy of Sciences, 55 Music Concourse Drive, San Francisco,

California 94118. Email: [email protected]

* Corresponding Author. Email: [email protected]

Abstract. A phylogeny of the species-rich clade of the Neotropical frog genus Leptodactylus sensu stricto is presented on the basis of a total evi-

dence analysis of molecular (mitochondrial and nuclear markers) and non-molecular (adult and larval morphological and behavioral characters)

sampled from > 80% of the 75 currently recognized species. Our results support the monophyly of Leptodactylus sensu stricto, with Hydrolaetare

placed as its sister group. The reciprocal monophyly of Hydrolaetare and Leptodactylus sensu stricto does not require that we consider Hydrolaetare

as either a subgenus or synonym of Leptodactylus sensu lato. We recognize Leptodactylus sensu stricto, Hydrolaetare, Adenomera, and Lithodytes as

valid monophyletic genera. Our results generally support the traditionally recognized Leptodactylus species groups, with exceptions involving only

a few species that are easily accommodated without proposing new groups or significantly altering contents. The four groups form a pectinate

tree, with the Leptodactylus fuscus group diverging first, followed by the L. pentadactylus group, which is sister to the L. latrans and L. melanonotus

groups. To evaluate the impact of non-molecular evidence on our results, we compared our total evidence results with results obtained from analy-

ses using only molecular data. Although non-molecular evidence comprised only 3.5% of the total evidence matrix, it had a strong impact on our

total evidence results. Only one species group was monophyletic in the molecular-only analysis, and support differed in 86% of the 54 Leptodac-

tylus clades that are shared by the results of the two analyses. Even though no non-molecular evidence was included for Hydrolaetare, exclusion of

that data partition resulted in that genus being nested within Leptodactylus, demonstrating that the inclusion of a small amount of non-molecular

evidence for a subset of species can alter not only the placement of those species, but also species that were not scored for those data. The evolu-

tion of several natural history and reproductive traits is considered in the light of our phylogenic framework. Invasion of rocky outcrops, larval

oophagy, and use of underground reproductive chambers are restricted to species of the Leptodactylus fuscus and L. pentadactylus groups. In con-

trast, larval schooling, larval attendance, and more complex parental care are restricted to the L. latrans and L. melanonotus groups. Construction

of foam nests is plesiomorphic in Leptodactylus but their placement varies extensively (e.g., underground chambers, surface of waterbodies, natu-

ral or excavated basins). Information on species synonymy, etymology, adult and larval morphology, advertisement call, and geographic distribu-

tion is summarized in species accounts for the 30 species of the Leptodactylus fuscus group, 17 species of the L. pentadactylus group, eight species

of the L. latrans group, and 17 species of the L. melanonotus group, as well as the three species that are currently unassigned to any species group.

Keywords. Behavior; Distribution; Life history; Morphology; Taxonomy; Vocalization.

Resumen. Se presenta una filogenia del género Leptodactylus, un clado neotropical rico en especies, basada en análises combinados de datos

moleculares (marcadores nuclear y mitocondriales) y no moleculares (caracteres de la morfología de adultos y larvas así como de comportamien-

to) se muestrearon > 80% de las 75 especies reconocidas. Los resultados apoyan la monofília de Leptodactylus sensu stricto, con Hydrolaetare

como su grupo hermano. La monofília recíproca de Hydrolaetare y Leptodactylus no requiere considerar a Hydrolaetare como un subgénero o si-

nónimo de Leptodactylus sensu lato. Se reconocen Leptodactylus sensu stricto, Hydrolaetare, Adenomera y Lithodytes como géneros monofiléticos

válidos. Los resultados en general resuelven los grupos tradicionalmente reconocidos de Leptodactylus, con excepciones de algunas especies que

son reasignadas sin la necesidad de proponer nuevos grupos o alterar significativamente el contenido de los grupos tradicionales. Los cuatro

grupos de especies forman una topología pectinada donde el grupo de L. fuscus tiene una posición basal, seguido por el grupo de L. pentadactylus

que es el grupo hermano al clado formado por los grupo de L. latrans y L. melanonotus. Se estimó el impacto de los datos no moleculares en los

resultados, comparándose los resultados de evidencia total con los de los análises de datos moleculares solamente. Los datos no moleculares

representan un 3.5% de la matriz de evidencia total, pero estos datos tuvieron un impacto significativo en los resultados del análisis de eviden-

cia total. En el análisis estrictamente molecular solamente un grupo de especies resultó monofilético, y el apoyo difirió en 86% de los 54 clados

de Leptodactylus compartidos entre los dos análises. A pesar que datos no moleculares no fueron incluídos para Hydrolaetare, la exclusión de

evidencia no molecular resultó en el género estar dentro de Leptodactylus, demostrando que la inclusión de evidencia no molecular pequeña para

un subgrupo de especies altera no solamente la posición topológica de esas especies, sino tambien de las especies para las cuales dichos datos

no fueron codificados. La evolución de patrones de historia natural y reprodución se evalúan en el contexto filogenético. La invasión de aflora-

mientos rocosos y la construción de cámaras de reprodución subterraneas está limitada a los grupos de Leptodactylus fuscus y L. pentadactylus,

mientras que la oofagia larval está restringida al grupo de L. pentadactylus. Por otro lado, los cárdumenes larvales, la proteción del cárdumen, y

otros comportamientos parentales complejos carecterizan al clado formado por los grupos de especies de L. latrans y L. melanonotus. Los resú-

menes de especies incluyen información de sinonímias, etimología, morfología de adultos y larvas, cantos, y distribución geográfica para las 30

especies del grupo de Leptodactylus fuscus, 17 especies del grupo L. pentadactylus, ocho especies del grupo de L. latrans, 17 especies del grupo de

L. melanonotus, así como para las tres especies que actualmente no se encuentran asociadas a ninguno de los grupos de especies.

South American Journal of Herpetology, 9(Special Issue 1), 2014, S1–S128

© 2014 Brazilian Society of Herpetology

Submitted: 07 July 2013

Accepted: 18 July 2014

Handling Editor: Marcio Martins

doi: 10.2994/SAJH-D-13-00022.1

CONTENTS

INTRODUCTION ........................................................................................................................................................................S4MATERIALS AND METHODS ...................................................................................................................................................S6

Ingroup delimitation and outgroup sampling .....................................................................................................................S6Molecular data and sampling................................................................................................................................................S6Non-molecular data and sampling .......................................................................................................................................S6Molecular methods ...............................................................................................................................................................S7Non-molecular characters and methods ..............................................................................................................................S7Phylogenetic analyses ...........................................................................................................................................................S8Other methods ......................................................................................................................................................................S8

RESULTS AND DISCUSSION .....................................................................................................................................................S9Overview and outgroup relationships..................................................................................................................................S9Ingroup monophyly and relationships ...............................................................................................................................S12

Leptodactylus fuscus group .............................................................................................................................................S14Leptodactylus pentadactylus group ................................................................................................................................S15Leptodactylus latrans group ...........................................................................................................................................S15Leptodactylus melanonotus group ..................................................................................................................................S16

The relevance of non-molecular evidence ..........................................................................................................................S16Evolution of Leptodactylus traits ........................................................................................................................................S19

Invasion of rocky outcrops ............................................................................................................................................S19Foam nest construction ................................................................................................................................................S19Parental care ..................................................................................................................................................................S20Larval oophagy ..............................................................................................................................................................S22

ACCOUNTS FOR SPECIES OF THE GENUS LEPTODACTYLUS FITZINGER, 1826 .............................................................S23Leptodactylus fuscus species group ......................................................................................................................................S24

Leptodactylus albilabris (Günther, 1859a) ....................................................................................................................S24Leptodactylus bufonius Boulenger, 1894 .......................................................................................................................S24Leptodactylus caatingae Heyer and Juncá, 2003 ...........................................................................................................S25Leptodactylus camaquara Sazima and Bokermann, 1978 .............................................................................................S26Leptodactylus cunicularius Sazima and Bokermann, 1978 ...........................................................................................S27Leptodactylus cupreus Caramaschi, Feio, and São Pedro, 2008 ....................................................................................S28Leptodactylus didymus Heyer, García-Lopez, and Cardoso, 1996 ................................................................................S29Leptodactylus elenae Heyer, 1978 ..................................................................................................................................S29Leptodactylus fragilis (Brocchi, 1877) ............................................................................................................................S30Leptodactylus furnarius Sazima and Bokermann, 1978 ...............................................................................................S31Leptodactylus fuscus (Schneider, 1799) .........................................................................................................................S32Leptodactylus gracilis (Duméril and Bibron, 1840) .......................................................................................................S34Leptodactylus jolyi Sazima and Bokermann, 1978 ........................................................................................................S35Leptodactylus labrosus Jiménez de la Espada, 1875 .....................................................................................................S36Leptodactylus laticeps Boulenger, 1918 .........................................................................................................................S36Leptodactylus latinasus Jiménez de la Espada, 1875 ....................................................................................................S37Leptodactylus longirostris Boulenger, 1882 ...................................................................................................................S38Leptodactylus marambaiae Izecksohn, 1976 .................................................................................................................S39Leptodactylus mystaceus (Spix, 1824) ............................................................................................................................S40Leptodactylus mystacinus (Burmeister, 1861) ...............................................................................................................S41Leptodactylus notoaktites Heyer, 1978 ..........................................................................................................................S42Leptodactylus oreomantis Carvalho, Fortes, Pezzuti, 2013 ..........................................................................................S43Leptodactylus plaumanni Ahl, 1936 ...............................................................................................................................S43Leptodactylus poecilochilus (Cope, 1862) .......................................................................................................................S44Leptodactylus sertanejo Giaretta and Costa, 2007 ........................................................................................................S45Leptodactylus spixi Heyer, 1983 .....................................................................................................................................S46Leptodactylus syphax Bokermann, 1969 .......................................................................................................................S46Leptodactylus tapiti Sazima and Bokermann, 1978......................................................................................................S47Leptodactylus troglodytes Lutz, 1926a ...........................................................................................................................S48Leptodactylus ventrimaculatus Boulenger, 1902 ...........................................................................................................S49

Systematics of the Neotropical Genus Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae):

Phylogeny, the Relevance of Non-molecular Evidence, and Species Accounts

Rafael O. de Sá, Taran Grant, Arley Camargo, W. Ronald Heyer, Maria L. Ponssa, Edward Stanley

S2


Leptodactylus pentadactylus species group..........................................................................................................................S49

Leptodactylus fallax Müller, 1926 ..................................................................................................................................S49

Leptodactylus flavopictus Lutz, 1926a ...........................................................................................................................S50

Leptodactylus knudseni Heyer, 1972 ..............................................................................................................................S51

Leptodactylus labyrinthicus (Spix, 1824) .......................................................................................................................S52

Leptodactylus lithonaetes Heyer, 1995 ...........................................................................................................................S53

Leptodactylus myersi Heyer, 1995 ..................................................................................................................................S54

Leptodactylus paraensis Heyer, 2005 .............................................................................................................................S55

Leptodactylus pentadactylus (Laurenti, 1768) ...............................................................................................................S55

Leptodactylus peritoaktites Heyer, 2005 ........................................................................................................................S57

Leptodactylus rhodomerus Heyer, 2005 .........................................................................................................................S58

Leptodactylus rhodomystax Boulenger, 1884 “1883” ....................................................................................................S59

Leptodactylus rhodonotus (Günther, 1869) ...................................................................................................................S59

Leptodactylus rugosus Noble, 1923 ................................................................................................................................S60

Leptodactylus savagei Heyer, 2005 ................................................................................................................................S61

Leptodactylus stenodema Jiménez de la Espada, 1875 .................................................................................................S62

Leptodactylus turimiquensis Heyer, 2005 ......................................................................................................................S63

Leptodactylus vastus Lutz, 1930 ....................................................................................................................................S63

Leptodactylus latrans species group ....................................................................................................................................S64

Leptodactylus bolivianus Boulenger, 1898 .....................................................................................................................S64

Leptodactylus chaquensis Cei, 1950................................................................................................................................S65

Leptodactylus guianensis Heyer and de Sá, 2011 ..........................................................................................................S67

Leptodactylus insularum Barbour, 1906 ........................................................................................................................S67

Leptodactylus latrans (Steffen, 1815) ............................................................................................................................S68

Leptodactylus macrosternum Miranda-Ribeiro, 1926 ...................................................................................................S69

Leptodactylus silvanimbus McCranie, Wilson, and Porras, 1980 ..................................................................................S70

Leptodactylus viridis Jim and Spirandeli-Cruz, 1973 ...................................................................................................S71

Leptodactylus melanonotus species group ...........................................................................................................................S71

Leptodactylus colombiensis Heyer, 1994 ........................................................................................................................S71

Leptodactylus diedrus Heyer, 1994 ................................................................................................................................S72

Leptodactylus discodactylus Boulenger, 1884 “1883” ....................................................................................................S73

Leptodactylus griseigularis (Henle, 1981) ......................................................................................................................S74

Leptodactylus leptodactyloides (Andersson, 1945) ........................................................................................................S75

Leptodactylus magistris Mijares-Urrutia, 1997.............................................................................................................S76

Leptodactylus melanonotus (Hallowell, 1861 “1860”) ...................................................................................................S77

Leptodactylus natalensis Lutz, 1930 ..............................................................................................................................S78

Leptodactylus nesiotus Heyer, 1994 ...............................................................................................................................S79

Leptodactylus pascoensis Heyer, 1994 ............................................................................................................................S79

Leptodactylus petersii (Steindachner, 1864) .................................................................................................................S80

Leptodactylus podicipinus (Cope, 1862) .........................................................................................................................S82

Leptodactylus pustulatus (Peters, 1870) ........................................................................................................................S83

Leptodactylus riveroi Heyer and Pyburn, 1983 .............................................................................................................S84

Leptodactylus sabanensis Heyer, 1994 ...........................................................................................................................S84

Leptodactylus validus Garman, 1888 .............................................................................................................................S85

Leptodactylus wagneri (Peters, 1862) ............................................................................................................................S87

Leptodactylus species not assigned to a species group.......................................................................................................S88

Leptodactylus hylodes (Reinhardt and Lütken, 1862) ...................................................................................................S88

Leptodactylus lauramiriamae Heyer and Crombie, 2005 ..............................................................................................S89

Leptodactylus ochraceus Lutz, 1930 ...............................................................................................................................S89

ACKNOWLEDGMENTS ...........................................................................................................................................................S89

REFERENCES ............................................................................................................................................................................S90

APPENDIX 1. GENBANK ACCESSION NUMBERS ...............................................................................................................S103

APPENDIX 2. NON-MOLECULAR CHARACTERS USED IN THE ANALYSES ...................................................................S106

APPENDIX 3. SPECIES EXAMINED FOR MORPHOLOGICAL DATA COLLECTION .........................................................S113

PLATES ....................................................................................................................................................................................S117




S3


INTRODUCTION

The Neotropical genus Leptodactylus Fitzinger, 1826

is a species-rich clade of Neotropical frogs ranging in size

from medium to very large (relative to most other Neo-

tropical anurans), some species are active foragers in the

leaf-litter (e.g., L. wagneri, Pough et al., 1992), whereas

some of the larger species are sit-and-wait predators found

around ponds (e.g., L. latrans, Strüssmann et al., 1984) or

sit outside burrows they occupy permanently (e.g., L. sav-

agei, reported as L. pentadactylus in Scott, 1983); Lepto-

dactylus species usually consume small invertebrate prey

(Rodrigues et al., 2004) but can also predate on anurans

as well as other small vertebrates (e.g., L. chaquensis, Duré,

1999; L. labyrinthicus; Vaz-Silva and da Frota 2003; L. lati-

ceps, Scott and Aquino, 2005).

The reproductive behavior of Leptodactylus is often

complex and has been studied extensively. Species of Lep-

todactylus have conspicuous advertisement calls to attract

females (e.g., L. mystacinus, Abrunhosa et al., 2001), male

aggressive and competitive calls (e.g., L. albilabris, Lopez

et al., 1988), female defensive calls (e.g., L. latrans, Vaz-

Ferreira and Gehrau, 1975), and distress calls (e.g., L. pen-

tadactylus, Hödl and Gollmann, 1986; L. chaquensis and

L. elenae, Padial et al., 2006); seismic communication has

also been reported in the genus (e.g., L. albilabris, Lewis

and Narins, 1985; L. syphax Cardoso and Heyer, 1995).

Some species have distinct sexual dimorphism with hy-

pertrophied forelimbs in males, sometimes accompanied

by sharp nuptial spines on the thumb (e.g., L. latrans, Cei,

1980; L. bolivianus complex, Heyer and de Sá, 2011). Com-

plex parental care has been reported in the genus, such as

the construction of distinct underground burrows (Arz-

abe and Prado, 2006) and foam nests in which embryos

develop; various forms of protection by the parents of the

foam nest and subsequently the larvae, including adults

actively attacking predators and emitting unique vocaliza-

tions (e.g., L. latrans, Vaz-Ferreira and Gehrau, 1975), and

tadpole schooling (e.g., L. chaquensis, Prado et al., 2000).

Furthermore, some species have evolved larval oophagy

(e.g., obligatory in L. fallax, Gibson and Buley, 2004) and

carnivory (e.g., facultative in L. savagei, Ruibal and Thom-

as, 1988), which play important functions in community

ecology (Allmon, 1991; Conte and Machado, 2005).

Some Leptodactylus species are a source of human

food (e.g., L. chaquensis, L. latrans [reported as L. ocel-

latus], Gallardo, 1979; L. fallax, Krintler, 1986), and the

dermal glands of several species are known to produce

defensive skin secretions (Cei et al., 1967), including an-

timicrobial peptides and other protein toxins found in

L. fallax (Rollins-Smith et al., 2005; King et al., 2005a),

L. labyrinthicus (Libério et al., 2014), L. laticeps (Conlon

et al., 2009), L. latrans (Nascimento et al., 2004, 2007;

Leite et al., 2010), L. pentadactylus (Habermehl, 1981;

Barlow, 1998; King et al., 2005b; Limaverde et al., 2009;

Sousa et al., 2009), L. syphax (Dourado et al., 2007). Simi-

larly, the foam nests of L. vastus possess a novel surfac-

tant protein (Hissa et al., 2008, 2014).

Leptodactylus is widely distributed across Neotropi-

cal lowlands from southern North America to southern

South America. The genus extends throughout South

America (on both sides of the Andes in northern South

America but restricted to the east of the Andes across

most of their distribution in South America) and over the

West Indies (Fig. 1). Leptodactylus is also ecologically di-

verse, occupying a wide range of environments from low-

land dense rainforests (primary and secondary rainforest)

to open habitats (including Savanna, Caatinga, Cerrado,

Chaco, and Grasslands, Ab’Sáber, 1977; Joly et al., 1999);

they are also found in artificial open habitats, previously

forested areas, and areas currently used for agriculture

and cattle ranching.

Although the clade (and even some species, e.g., Lep-

todactylus fuscus) extends over an impressive latitudinal

range, its elevational range is generally more restricted.

Leptodactylus is a predominantly lowland clade with most

species occurring below 2,000 m. A few species occur and

reproduce above 1,000 m sea level (e.g., L. furnarius, L. la-

trans in Serra da Bocaina, Rio do Janeiro and São Paulo

states, Brazil) or at 1,300–1,600 m (e.g., L. syphax, L. laby-

rinthicus, L. latrans, L. jolyi, L. fuscus, L. cunicularius, and

L. camaquara in Serra do Cipó, Minas Gerais state, Bra-

zil). However, L. colombiensis extends from lowland areas

Figure 1. Geographic distribution of the genus Leptodactylus (shown in

gray).




S4


to 2600 m in the northern Andes of Colombia, whereas

L. silvanimbus is restricted to the high altitude cloud for-

ests of Honduras from 1700–1900 m.

Although some Leptodactylus species occur at con-

siderable distances from water sources throughout the

year, most species are strongly associated with water bod-

ies; some species are associated primarily or exclusively

with lotic systems (e.g., streams and creeks of riparian

environments) and others associated with lentic systems

(e.g., lakes, permanent and annual ponds, smaller ephem-

eral pools, and artificial water sources). Until recently,

the fossil record for the genus was limited to remains of

extant or indeterminate species from the Quaternary of

Mexico, Bolivia, Brazil, Uruguay, Argentina, and the West

Indies (Vergnaud-Grazzini, 1968; Lynch, 1971; Mones,

1975; Pregill, 1981; Van Devender et al., 1985; Lezcano

et al., 1993; Sanchiz, 1998). However, the history of the

genus was extended back to the early Pliocene of Argenti-

na (Farola Monte Hermoso, Buenos Aires Province) based

on fossils remains considered close to L. latrans (Gómez

et al., 2013).

The systematic documentation of the diversity of

the genus Leptodactylus began in 1826 when Fitzinger

erected the genus, provided a key to the known species,

and described three new species (Fitzinger, 1826). Since

then and until about the middle of the 20th century, taxo-

nomic activity on the group mainly consisted of species

descriptions. The last six decades have seen a rapid rate

of discovery and description of new species (including

> 40% of the 75 currently known species), as well as the

reevaluation of species limits and relationships and nu-

merous nomenclatural synonymies and resurrections.

Current understanding of Leptodactylus systemat-

ics and diversity is derived primarily from the works of

W.R. Heyer and collaborators over the last four decades;

a bibliography of the genus was recently published (Heyer

et al., 2009a, b). Two papers in particular have influenced

the understanding of the genus taxonomy. First, Heyer

(1969a) redefined the genus and described the monotypic

genus Barycholos for L. pulcher. Second, Heyer (1969b)

clustered Leptodactylus species based on their overall eco-

logical characteristics into five species groups, the L. fus-

cus, L. marmoratus, L. melanonotus, L. ocellatus (= L. la-

trans; Lavilla et al., 2010), and L. pentadactylus groups.

Subsequent research, much of it by Heyer and collab-

orators, resulted in taxonomic contributions that docu-

mented the diversity of the genus. The 1970s witness the

osteological characterization of the genus in the context

of all other leptodactyloid frogs (Lynch, 1971), revision of

the L. melanonotus group (Heyer, 1970a), the L. pentadac-

tylus group (Heyer, 1972), and the L. fuscus group (Heyer,

1978), and recognition of the monotypic genus Vanzo-

linius to accommodate L. discodactylus (Heyer, 1974a),

as well as the resurrection of Adenomera Steindachner

1867 for the L. marmoratus group (Heyer, 1974b). In the

1980s, Heyer and Maxson (1982) and Maxson and Heyer

(1988) assessed relationships among the species groups

of Leptodactylus sensu Heyer (1974a) using immuno-

logical distances. In the 1990s, Heyer (1994) revised the

L. podicipinus-wagneri species complex within the L. mela-

nonotus group and Heyer et al. (1996a) analyzed, but did

not diagnose, the L. mystaceus species complex within the

L. fuscus group.

In the 21st Century, anuran systematics and taxon-

omy has progressed rapidly based on both molecular and

detailed morphological studies (Haas, 2003; Faivovich

et al., 2005; Frost et al., 2006; Grant et al., 2006; Van der

Meijen et al., 2007; Pyron and Wiens, 2011; de Sá et al.,

2012). Vanzolinius discodactylus was returned to Leptodac-

tylus (de Sá et al., 2005a; Frost et al., 2006) and Frost et al.

(2006) also returned the species of Adenomera, along with

the monotypic Lithodytes Fitzinger, 1843, to Leptodacty-

lus, a taxonomic group we refer to as Leptodactylus sensu

lato. Although that taxonomic arrangement has not been

followed universally (e.g., Kwet et al., 2009), it also has

not been rejected by phylogenetic analysis. As such, below

we refer to the group composed of Leptodactylus sensu

Heyer (1969a, b), i.e., excluding the L. marmoratus group

and L. lineatus but including Vanzolinius, as Leptodactylus

sensu stricto. Ponssa (2008) performed a cladistic analy-

sis of the L. fuscus group and subsequently expanded the

morphological matrix by adding data from Heyer et al.

(1998) and new evidence from L. nesiotus (Ponssa et al.,

2010). Heyer and de Sá (2011) revised the L. bolivianus

species complex. Recently, Miranda et al. (2014) built on

Larson and de Sá’s (1998) analysis of internal larval mor-

phology and combined it with a subset of the characters

from Ponssa (2008) and Ponssa et al. (2010).

Perhaps of greatest importance, over the nearly

half-century since Heyer’s first contributions, the known

diversity of Leptodactylus s.s. has grown from the 24 spe-

cies listed in Heyer (1969a) to 75 species known currently,

which has had a profound impact on understanding of the

diversity and evolution of this clade.

Although the last 50 years have witnessed an un-

deniable increase in understanding of the systematics of

Leptodactylus, information is scattered across numerous

articles and is derived from analyses of limited datasets

that consider only a fraction of the known diversity of the

clade. As such, in this paper we analyze a large dataset

composed of mitochondrial and nuclear DNA sequences

and morphological and behavioral data for species of

Leptodactylus s.s. and a large outgroup sample in order to

(1) provide a species level phylogeny for Leptodactylus s.s.,

(2) evaluate the monophyly of the traditionally recognized

species groups, and (3) determine the closest relatives to

Leptodactylus s.s. To facilitate future studies of this fasci-

nating clade of Neotropical frogs, we also provide species

accounts for all known species of Leptodactylus s.s., assess

the behavioral evolution in the clade, and evaluate the




S5


effects of a modest matrix of non-molecular characters on

an analysis dominated by DNA sequence data.

MATERIALS AND METHODS

Ingroup delimitation and outgroup sampling

We defined Leptodactylus s.s. as the ingroup for this

study and sampled outgroup terminals specifically to test

the monophyly of Leptodactylus s.s. and the polarity of

the states of the ingroup root node. To that end, we tar-

geted taxa previously recovered as closely related to the

ingroup (Frost et al., 2006; Grant et al., 2006; Lourenço

et al., 2008; Pyron and Wiens, 2011). We included species

of Leptodactylus s.l., including three (one undescribed) of

the 18 species of the L. marmoratus group (= Adenomera)

and L. lineatus, the sole member of the L. lineatus group

(= Lithodytes), and representatives of all other leptodac-

tylid genera, including two of the three species of Hydro-

laetare, Scythrophrys sawayae (the sole representative of

the genus), and three of the seven recognized species of

Paratelmatobius, as well as three more apparently unde-

scribed species of that genus.

The inclusion of Leptodactylidae within Athesphat-

anura is non-controversial; therefore we restricted our

sampling to that clade and included the non-athesphat-

anuran taxa Hemiphractus helioi (Hemiphractidae) and

Craugastor rhodopis (Terrarana, Craugastoridae) to di-

rect the topology. In contrast, the precise sister-group

of Leptodactylidae among athesphatanurans is highly

controversial; consequently, we included numerous spe-

cies of each of the potential sister clades. Grant et al.

(2006) found leiuperids and leptodactylids to be distantly

related; however, other studies found them to be closely

related and treated them as members of the same family

(Frost et al., 2006) or subfamily (Pyron and Wiens, 2011).

Moreover, we included a large number of leiuperids in our

sample of outgroup taxa, including 10 species of Engys-

tomops (including two undescribed species), 9 species of

Physalaemus, and 1 species each of Edalorhina, Pleurode-

ma, and Pseudopaludicola. Several studies (e.g., Frost et al.,

2006; Guayasamin et al., 2009) have found centrolenids

and Allophryne ruthveni (variably treated as a centrolenid

or as a separate family) to be sister to Leptodactylidae

whereas others (e.g., Grant et al., 2006; Pyron and Wiens,

2011) recovered different sister-group relationships but

still found them to be in the same vicinity as leptodac-

tylids. As such, we included Allophryne ruthveni and sev-

en species from across the diversity of centrolenids (in-

cluding Centrolene grandisonae, Espadarana prosoblepon,

Nymphargus bejaranoi, N. garciae, Vitreorana eurygnatha,

and an unidentified specimen of Hylalinobatrachium).

Additionally, we included a representative sample of ple-

siomorphic bufonids (four species), ceratophryids (seven

species), cycloramphids (six species), hemiphractids (two

species), hylids (two species), hylodids (three species),

and one dendrobatid.

Given our objectives, taxon sampling, and evidence

(molecular and non-molecular characters), our analy-

ses were intended to test the relationships of Leptodac-

tylus s.s. and were not designed to test the relationships

among the outgroup taxa proposed in previous studies

(e.g., Frost et al., 2006; Grant et al., 2006; Pyron and

Wiens, 2011).

Molecular data and sampling

To address the relationships of Leptodactylus s.s.,

we targeted the large (16S) and small (12S) mitochon-

drial ribosomal subunits and the nuclear gene rhodopsin.

Voucher information for molecular data are provided in

Appendix 1. DNA sequences were obtained for all includ-

ed outgroup taxa. Our ingroup included 62 of the 75 cur-

rently recognized species (83%) of Leptodactylus s.s. We

included DNA sequences for all 6 of the 7 species (85%)

of the L. latrans group (not included L. guianensis) 24 of

the 28 species (86%) of the L. fuscus group (not included:

L. caatingae, L. cupreus, L. oreomantis, and L. spixi), 16 of

the 18 species (89%) of the L. pentadactylus group (not

included: L. rhodomerus and L. turimiquensis), and 13 of

the 16 species (81%) of the L. melanonotus group (not in-

cluded: L. magistris, L. pascoensis, and L. sabanensis). We

also included DNA sequences for L. lithonaetes, L. riveroi,

L. silvanimbus, and L. viridis, which previously were not

strongly associated with any species group. We were un-

able to include L. lauramiriamae (not associated with any

species group), L. hylodes (known only from the lectotype,

Heyer, 2000), and L. ochraceus (known only from the holo-

type, Caramaschi, 2008). We included multiple terminals

for ingroup taxa known or suspected to be species com-

plexes, as well as conspecifics collected at disparate locali-

ties. In total, our ingroup included 81 terminals of Lepto-

dactylus s.s. The following species are considered not to

belong to the genus Leptodactylus: Hylodes hallowelli Cope,

1862 and Plectomantis rhodostima Cope, 1874.

Non-molecular data and sampling

Morphological and behavioral characters were taken

from Ponssa (2008) and Ponssa et al. (2010) and also in-

clude 21 additional characters (characters 8, 29, 30–31,

33, 35–36, 40, 45–49, 51, 56–60, and 69–71; Appendix 2).

Unfortunately, our study was already accepted for publi-

cation prior to the publication of Miranda et al. (2014),

so we were unable to include that data. Locality data and

catalog numbers for specimens examined are provided

in Appendix 3. These characters were included for 61 of




S6


the 62 nominal species (not included: L. sertanejo of the

L. fuscus group).

Non-molecular sampling of the outgroup taxa was

limited to Leptodactylus lineatus (= Lithodytes), L. hylae-

dactylus of the L. marmoratus group (= Adenomera), Scyth-

rophrys sawayae (data from Verdade, 2005), Paratelmato-

bius lutzi, and Engystomops pustulosus.

Molecular methods

Total genomic DNA was extracted with DNeasy

Tissue Kits (Qiagen, Valencia, CA) from liver or thigh

muscle that was preserved in ethanol 95%. Fragments

of the 12S ribosomal RNA (rRNA), 16S rRNA, and rho-

dopsin genes were PCR amplified (Palumbi, 1996) using

an MJ Research PTC-200 thermocycler. Double-strand-

ed PCR amplifications were executed with 25 μl of Pro-

mega Master Mix (Promega, Madison, WI), 23 μl of pu-

rified water, 0.4 μl of forward and reverse primers, and

approximately 0.5–2 μl of DNA (depending on strength

of DNA isolation). A segment of about 900 base pairs

(bp) from the 12S rDNA gene was amplified with prim-

ers 12Sa 5’-AAACTGGGATTAGATACCCCACTAT-3’,

12Sb 5’-GAGGGTGACGGGCGCTGTGT-3’, 12S Tphef

5’-ATAGC(A/G)CTGAA(A/G)A(C/T)GCT(A/G)AGATG-3’,

and 12S RdS1 5’-GGTACCGTCAAGTCCTTTGGGTT-3’

using the following thermal conditions: initial 94°C for

2 min followed by 30 cycles of 94°C for 1, 53°C for 1 min,

and 72°C for 1.5 min. A segment of about 800 base pairs

(bp) from the 16S rDNA gene was amplified with primers

16S L2A 5’-CCAAACGAGCCTAGTGATAGCTGGTT-3’, 16S

Ar 5’-CGCCTGTTTACCAAAAACAT-3’, and 16S Br 5’-CTC-

CGGTCTGAACTCAGATCACGTAG-3’ under the following

thermal conditions: initial denaturation at 94°C for 2 min

followed by 34 cycles of 94°C for 1.5 min, 58°C for 1 min,

and 72°C for 1.5 min. A segment of about 310 bp from the

rhodopsin nuclear gene was amplified with primers Rhod

1A/D (Hoegg et al., 2004) with the following conditions:

94°C for 2 min, 49°C for 1 min, and 72°C for 1 min, fol-

lowed by 34 cycles of 94°C for 1 min, 49°C for 1 min, 72°C

for 1 min, and one final cycle of 72°C for 6 min.

Amplified segments were purified using Exo-Sap

(USB) by heating samples at 80°C for 15 min. Purified

products were cycle-sequenced with the dideoxy chain

termination method using the Sequi-Therm Excel II DNA

sequencing kit (Epicentre Technologies). Infrared-labeled

sequencing primers (same as amplification primers) were

used in sequencing reactions (Li-Cor Biotechnology) un-

der the following thermal conditions: initial denaturation

at 95°C for 2.5 min, followed by 30 cycles of 95°C for 30 s,

58°C for 30 s, and 70°C for 30 s. Sequencing products

were run in 6% acrylamide, 44 cm in length, gels using a

Li-cor DNA 4300 automatic sequencer at the University

of Richmond. Sequencing reactions were single stranded;

double-stranded PCR fragments were sequenced in both

directions. Complementary sequence strands for each

sample were first aligned and, using the chromatographs

created by BaseImagr software (Li-cor Biotechnology),

were inspected visually for mismatches of aligned posi-

tions to confirm or manually correct the automatic nucle-

otide reading. Sequences included in the analyses repre-

sent a consensus of both DNA strands.

Locality data for specimens included in the molecu-

lar analyses as well as GenBank accession numbers for se-

quences generated in this study are given in Appendix 1.

Non-molecular characters and methods

Skeletal characters were scored in specimens dou-

bled-stained for cartilage and bone with alcian blue and

alizarin red following Wassersug (1976). Prior to stain-

ing, specimens were rehydrated, eviscerated, and washed

in distilled water; the duration of each step varied due to

the size of the specimens. Dry skeletons and digital X-rays

also were analyzed. All observations were made with a

Carl Zeiss Discovery V8 stereo dissection microscope.

Measurements were taken with a digital caliper (Mitu-

toyo CD-30C and CD-15B; ± 0.01 mm), or with Image

Tool software on digital images taken with a 5-megapixel

digital camera. Terminology follows Trueb (1973) and

Trueb et al. (2000) for cranial and postcranial characters,

Maglia et al. (2007) and Pugener and Maglia (2007) for

the olfactory region, and Trewavas (1933) for laryngeal

morphology.

Behavioral characters were scored based on data

from many studies, including Cei (1949a, b, 1980), Gal-

lardo (1958, 1964a), Sexton (1962), Heatwole et al.

(1965), Pisanó and Barbieri (1965), Heyer and Silver-

stone (1969), Lescure (1972, 1979), Barrio (1973), Heyer

and Bellin (1973), Heyer (1974a, b; 1978), Philibosian

et al. (1974), Muedeking and Heyer (1976), Heyer and

Rand (1977), Toft and Duellman (1979), Downie (1984,

1989, 1990, 1994, 1996), Lescure and Letellier (1983),

Aichinger (1985), Solano (1987), Martins (1988), Wells

and Bard (1988), Caldwell and Lopez (1989), Gascon

(1991), Rodriguez (1992), Pisanó et al. (1993), Rodrí-

guez and Duellman (1994), Cardoso and Heyer (1995),

De la Riva (1995, 1996), Lamar and Wild (1995), Vaira

(1997), Prado et al. (2000), Freitas et al. (2001), Lewis

et al. (2001), Ponssa (2001), Almeida and Angulo (2002),

Prado et al. (2002), Prado and Haddad (2003), Readin and

Jofré (2003), França et al. (2004), Giaretta and Kokubum

(2004), Gibson and Buley (2004), Toledo et al (2005), da

Silva et al (2005), de Carvalho (2005), Oliveira Filho et al.

(2005), Kokubum and Giaretta (2005), Santos and Amor-

im (2005, 2006), Muniz and da Silva (2005), Prado et al.

(2005), Prado and Haddad (2005), Shepard and Caldwell

(2005), Tozetti and Toledo (2005), Zina and Haddad




S7


(2005), Arzabe and Prado (2006), Fenolio et al. (2006),

Giaretta and Oliveira Filho (2006), Siqueira et al. (2006),

Lucas et al. (2008), Ponssa and Barrionuevo (2008), Silva

and Giaretta (2008), da Silva and Giaretta (2009), Olivei-

ra Filho and Giaretta (2009), Giaretta and Facure (2009),

Kokubum et al. (2009), Schlüter et al. (2009).

Phylogenetic analyses

We performed a total evidence analysis (Kluge,

1989, 2004) of the molecular and non-molecular data

under the parsimony optimality criterion, applying equal

weights to all transformations. On the basis of the argu-

ments of Padial et al. (2014), we employed tree-alignment

(e.g., Sankoff, 1975; Wheeler, 1996; Varón and Wheeler,

2012, 2013) in POY 4.1.3 (Varón et al., 2010), which

tests hypotheses of nucleotide homology dynamically

by optimizing unaligned DNA sequences directly onto

alternative topologies (Kluge and Grant, 2006; Wheeler

et al., 2006; Grant and Kluge, 2009) while simultaneously

optimizing prealigned transformation series as standard

static matrices.

Following the rationale of Grant et al. (2006:56–57),

we treated each sequenced individual as a separate ter-

minal and duplicated the non-molecular data coded for

the species as a whole for each conspecific terminal ML

Comment. Although we maintain that the total evidence

analysis of all available evidence identifies the optimal

explanation (Kluge, 1989, 2004), we also analyzed the

molecular data separately using the same parameters in

order to evaluate the effect of a small morphological ma-

trix when combined with a larger DNA sequence dataset

(see below).

Analyses were run on the Museu de Zoologia da

Universidade de São Paulo’s high-performance comput-

ing cluster, Ace, which consists of 12 quad-socket AMD

Opteron 6376 16-core 2.3-GHz CPU, 16 MB cache,

6.4 GT/s compute nodes (= 768 cores total), eight with

128 GB RAM DDR3 1600 MHz (16 × 8 GB), two with

256 GB (16 × 16 GB), and two with 512 GB (32 × 16 GB),

and QDR 4x InfiniBand (32 GB/s) networking. For both

the total evidence and molecular-only datasets, we per-

formed the following analyses. First, using the standard

direct optimization algorithm (Wheeler, 1996), we ran 10

6-hr searches on 644 CPUs (giving a total of 38,400 CPU-

hours) using the command “search”, which implements

a driven search composed of random addition sequence

Wagner builds, Subtree Pruning and Regrafting (SPR) and

Tree Bisection and Reconnection (TBR) branch swapping

(RAS + swapping; Goloboff, 1996), Parsimony Ratcheting

(Nixon, 1999), and Tree Fusing (Goloboff, 1999), storing

the shortest trees from each independent run and per-

forming a final round of Tree Fusing on the pooled trees.

Next, using the approximate iterative pass algorithm

(Wheeler, 2003a), we read the optimal trees found in all

of previous analyses and swapped the optimal tree(s) to

completion. We then used the exact iterative pass algo-

rithm to calculate the cost of the optimal tree(s) from

the approximate iterative pass analysis and generate the

matrix version of the tree-alignment (i.e., the implied

alignment; Wheeler, 2003b). Finally, we performed 1,280

RAS + TBR of the implied alignment to verify the length

reported by POY and search for additional optimal trees.

We estimated clade support (Grant and Kluge,

2008a) using the Goodman-Bremer measure (GB; Good-

man et al., 1982; Bremer, 1988; Grant and Kluge, 2008b)

by determining the length difference between the optimal

tree and all trees visited during a TBR swap of the mini-

mum length tree. To accelerate GB analyses, we calculated

tree lengths using the implied alignment of the optimal

topology. Although shorter suboptimal trees might be

found by calculating the optimal tree-alignment for each

visited topology, Padial et al. (2014) found that this ap-

proach overestimates GB values significantly less than

when GB is calculated using a MAFFT (Katoh et al., 2005)

similarity-alignment.

To evaluate the impact of the small non-molecular

dataset on our results, we repeated all analyses using

only the molecular dataset. We assessed differences by

examining clade-by-clade differences and by calculating

the pairwise rooted SPR distances between the optimal

molecular-only and total evidence topologies using the

method of Goloboff (2008; replicates = 50, stratification

level = 20) in the program TNT (Goloboff et al., 2008). In

order to meaningfully compare the GB values obtained in

the two analyses, for selected clades shared by both re-

sults we calculated the ratio of explanatory power (REP)

value (Grant and Kluge, 2007), which scales the observed

support for a given clade relative to its maximum pos-

sible support (Grant and Kluge, 2010). We obtained the

lengths of least parsimonious trees by conducting 1,152

random addition sequence + TBR searches with all charac-

ters assigned a weight of -1 and taking the absolute value

of the resulting lengths. To make REP values more man-

ageable, we multiplied them by 10,000 and report them to

two significant figures.

Other methods

Institutional acronyms for specimen repositories

follow Sabaj Pérez (2010), with the following exceptions.

AL-MN, The Adolfo Lutz amphibian collection is main-

tained separately from the MNRJ herpetology collec-

tion within the Museu Nacional, Rio de Janeiro; CHINM,

Dr. Avelino Barrio described a new species Leptodactylus

geminus (currently a synonym of L. plaumanni; Kwet et al.,

2001) with the holotype given as CHINM 5860. The holo-

type has since been transferred to the Museo Nacional de




S8


Ciencias Naturales, Buenos Aires, Argentina but retains

the original specimen number (J. Faivovich, pers. comm.).

EHT: Edward H. Taylor (1937 “1936”) described the spe-

cies Leptodactylus occidentalis using his field tag number

for the holotype, now deposited in the Field Museum of

Natural History and bears the number FMNH 100015

(Marx, 1976). WCAB, Werner C.A. Bokermann amassed

an extensive private amphibian collection identified by

his initials (WCAB). After Bokermann’s death, Paulo E.

Vanzolini at the Museu de Zoologia da Universidade de

São Paulo (MZUSP) purchased the Bokermann collection

and replaced all of the WCAB specimen tags with MZUSP

tags.

Species accounts are first arranged according to the

species groups as defined in this paper based on our phy-

logenetic analyses and second in alphabetical order with-

in each species group. Adult size categories (small, medi-

um, large) follow the definitions of Heyer and Thompson

(2000). Mean size of adult males and females is not re-

ported for small sample sizes. Several of the characters

used in the adult morphology and similar species sections

utilize three terms that form a subjectively divided con-

tinuum of meaning: (1) distinct: that which may be clear-

ly seen, conspicuous; (2) indistinct: not clear, difficult to

distinguish, inconspicuous; (3) indiscernible: not discern-

ible, imperceptible, undistinguishable, apparently absent.

Brief descriptions of external larval morphology are

provided for each species, but do not include all available

descriptions for the same species. Tadpole stages fol-

low Gosner (1960). Oral disc terminology follows Altig

(1970). Additional references on reproduction and tad-

pole descriptions and anatomy are provided in Heyer et al.

(2009a, b). Recordings are housed at the USNM, Depart-

ment of Vertebrate Zoology, Division of Amphibians and

Reptiles (numbers of analyzed cuts are provided in the

figure legends). Call waveforms and spectrograms (using

256 point fast Fourier transform) were generated using

Raven Pro v.1.4 (Bioacoustics Research Program, 2011).

Dermal folds vary considerably in species of Lepto-

dactylus, which is often useful in species determination.

A total of seven fold (or fold-like) structures occur in the

genus (Fig. 2). Three of the folds are described in the adult

morphology sections of the species accounts: dorsal folds,

dorsolateral folds, and lateral folds. Additional fold in-

formation is used in the ‘Similar Species’ sections where

the fold information differentiates species. Folds may be

complete (= entire), interrupted, or a combination of both

complete and interrupted. The mid-dorsal fold we refer

to as “dorsal fold 1” is typically a row of small spines or

tubercles and is not strictly a dermal fold.

RESULTS AND DISCUSSION

Overview and outgroup relationships

Driven searches using the standard direct optimiza-

tion algorithm completed 21,428 replicates of random ad-

dition sequence builds + branch swapping, 45,530 rounds

of tree-fusing, and 8,334 iterations of ratcheting, result-

ing in a tree of 16,572 steps. Swapping using the approxi-

mate iterative pass algorithm further resulted in a tree of

16,517 steps, which was further reduced to 16501 steps

using the exact iterative pass algorithm; 1,280 replicates

of random addition sequence builds + branch swapping

did not identify a shorter tree. The strict consensus of

the 27 minimum length trees (Figs. 3A, B) collapses only

two ingroup nodes, resulting in the following polytomies

(Fig. 3A): (1) three of the Leptodactylus fuscus samples and

(2) the three L. labyrinthicus samples. Goodman-Bremer

values were calculated using the 585,173 trees visited

during the TBR swap of one of the optimal trees. The least

parsimonious tree (used for calculating REP values) was

35,895 steps.

We recovered a monophyletic Hydrolaetare Gal-

lardo, 1963 (type species: Limnomedusa schmidti Cochran

and Goin, 1959, by original designation) nested within

Leptodactylus s.l. as the sister group of Leptodactylus s.s.

(Fig. 3A). This placement agrees with the results of Fou-

quet et al. (2013), although those authors indicated that

adequate sampling within Leptodactylus, Adenomera, and

Hydrolaetare was needed to test the monophyly of these

genera. Our results also agree with Jansen et al. (2011),

although only if their neighbor-joining tree is re-rooted on

any leiuperid instead of within Leptodactylus. The close re-

lationship between Hydrolaetare and Leptodactylus is not

unexpected. Lynch (1971:177) remarked on the “striking

similarity between Hydrolaetare and Leptodactylus (ocel-

latus [= latrans] and pentadactylus groups)” and empha-

sized that the “otic plate of Hydrolaetare is small and like

that seen in the melanonotus, ocellatus, and pentadactylus Figure 2. Diagram of skin folds found in Leptodactylus. (Illustration by

WRH).




S9


20

21

20

16

6

3

9

13

13

31

27

2027

1324

35

13

18

46

20

41

22

38

15

1025

14

29

6

236

12

40

8

7

19

9

31

13

3

14

14

24

22

11

27

35

30

11

10

42

21

17

4

13

112

1760

13

11

8

2

3713

87

87

20

27

6

70

35

71

A

Hemiphractus helioi

Craugastor rhodopis

Allobates alagoanus

Thoropa miliaris

Rhinoderma darwinii

Eupsophus calcaratus

Alsodes gargola

Crossodactylus schmidti

Megaelosia goeldii

Hylodes phyllodes

Limnomedusa macroglossa

Pleurodema brachyops

Pleurodema brachyops

Melanophryniscus klappenbachi

Atelopus spurrelli

Rhaebo haematiticus

Amazophrynella minuta

Odontophrynus achalensis

Stefania evansi

Gastrotheca megacephala

Cycloramphus boraceiensis

*Scythrophrys sawayae

Paratelmatobius gaigeae

Paratelmatobius poecilogaster

Paratelmatobius

Paratelmatobius

Paratelmatobius

Paratelmatobius cardosoi

Batrachyla leptopus

Atelognathus patagonicus

Telmatobius jahuira

Telmatobius marmoratus

Lepidobatrachus laevis

Chacophrys pierottii

Ceratophrys cranwelli

Allophryne ruthveni

Hyalinobatrachium

Hyalinobatrachium fleischmanni

Hyalinobatrachium eurygnathum

Espadarana prosoblepon

Nymphargus grandisonae

Nymphargus

Nymphargus bejaranoi

Pseudopaludicola falcipes

Pseudopaludicola falcipes

Edalorhina perezi

Edalorhina perezi

Physalaemus albonotatus

Physalaemus enesefae

Physalaemus cuvieri

Physalaemus riograndensis

Physalaemus biligonigerus

Physalaemus barrioi

Physalaemus gracilis

Physalaemus nattereri

Physalaemus signifer

*Engystomops pustulosus

Engystomops petersi

Engystomops freibergi

Engystomops

Engystomops

Engystomops pustulatus

Engystomops randi

Engystomops montubio

Engystomops guayaco

Engystomops coloradorum

Phyllomedusa vaillanti

Hypsiboas boans

*Lithodytes lineatus

*Lithodytes lineatus

Adenomera hylaedactyla

Adenomera lutzi

Adenomera

*Adenomera hylaedactyla

Hydrolaetare dantasi

Hydrolaetare caparu

1

2

sp2

sp

sp3

sp

sp

1

2

1

2

cf

spD

spB

1

2

1

sp

2

Leptodactylus (Fig. 3B)

Figure 3. Strict consensus of 27 most parsimonious trees (16,501 steps) from the total evidence analysis. (A) Outgroup relationships. (B) Ingroup

relationships (on following page). Values below branches are Goodman-Bremer support and above branches are REP support. Terminals coded for non-

molecular characters are marked with an asterisk (*). Red = L. fuscus species group, green = L. pentadactylus species group, orange = L. latrans species group,

blue = L. melanonotus species group.




S10


*Leptodactylus syphax*Leptodactylus laticeps*Leptodactylus ventrimaculatus*Leptodactylus labrosus*Leptodactylus bufonius*Leptodactylus troglodytes*Leptodactylus mystacinus*Leptodactylus albilabris*Leptodactylus fragilis*Leptodactylus poecilochilus*Leptodactylus longirostris*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus latinasus*Leptodactylus gracilis

Leptodactylus sertanejo*Leptodactylus joyli*Leptodactylus tapiti*Leptodactylus plaumanni*Leptodactylus marambaiae*Leptodactylus cunicularis*Leptodactylus furnarius*Leptodactylus camaquara*Leptodactylus didymus*Leptodactylus mystaceus*Leptodactylus elenae*Leptodactylus notoaktites

Leptodactylus mystaceusLeptodactylus mystaceus

*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus fuscus*Leptodactylus lithonaetes*Leptodactylus rugosus*Leptodactylus rhodonotus*Leptodactylus rhodomystax*Leptodactylus flavopictus*Leptodactylus stenodema*Leptodactylus vastus*Leptodactylus paraensis*Leptodactylus myersi*Leptodactylus peritoaktites*Leptodactylus savagei*Leptodactylus pentadactylus*Leptodactylus knudseni*Leptodactylus fallax*Leptodactylus labyrinthicus*Leptodactylus labyrinthicus

Leptodactylus labyrinthicus*Leptodactylus silvanimbus*Leptodactylus insularum*Leptodactylus bolivianus*Leptodactylus viridis*Leptodactylus latrans*Leptodactylus latrans*Leptodactylus latrans*Leptodactylus chaquensis*Leptodactylus macrosternum*Leptodactylus macrosternum*Leptodactylus riveroi*Leptodactylus melanonotus*Leptodactylus wagneri*Leptodactylus colombiensis*Leptodactylus validus continetal*Leptodactylus validus*Leptodactylus validus*Leptodactylus validus*Leptodactylus nesiotus*Leptodactylus pustulatus*Leptodactylus natalenis*Leptodactylus petersii*Leptodactylus leptodactyloides*Leptodactylus grisegularis*Leptodactylus discodactylus*Leptodactylus podicipinus*Leptodactylus diedrus

Leptodactylus juvenile

1

2

3

4

5

1

2

3

6

7

8

9

1

2

3

2

NEOTYPE

1

1

2

1

2

3

sp

B

24

12

12

16

8.2

8.2

6

3.1

3.1

3.1

3.1

5.7

5.7

19

9.8

9.8

14

7.2

5

2.62.6

2.6

2.6

8

4.1

4.1

4.1

15

10

9

14

7.2

7.2

14

13

6.7

4

1

0.5

0.5

18

9.3

7

15

3

1.5

1.5

1.5

1.5

1.5

1.5

1.5

4

3

3

5

132

1.0

3

32

17

6

6

9

4.6

4.6

4.6

4.6

4.6

11

11

5.7

5.7

15

42

22

33

17

5

18

8.8

25

13

17

8.8

9

4

2.1

2.1

2.1

2.1

416

10

5.2

5.2

15

7.7

7.7

7.7

7.7

7.7

6

22

11

41

21

27

14

39

20

31

15

13

6.7

6.7

6.7

16

8.2

8.2

8.2

13

6.7

6.7

8

7

3.6

3.6

3.6

24

3

9

14

7.2

19

8

16

26

13

11

16

11

7

12

6.2

5

13

3

30

15

9

13

45

23




S11


groups of Leptodactylus.” Hydrolaetare currently consists

of three recognized species; variation on external mor-

phology and coloration was recently reported for the spe-

cies (Ferrão et al., 2014).

Given the placement of Hydrolaetare as the sister of

Leptodactylus s.s., one alternative is to place Hydrolaetare

within Leptodactylus as either a junior synonym of Lepto-

dactylus s.s. or a subgenus within Leptodactylus s.l. Insofar

as this would require the least perturbation to the current

taxonomy, this option is attractive. Furthermore, treat-

ing Hydrolaetare as a junior synonym of Leptodactylus s.s.

would be consistent with our analysis of the molecular data

(see below). However, Hydrolaetare is a morphologically

diagnosable (e.g., Lynch, 1971; Souza and Haddad, 2003)

genus that has been recognized consistently since it was

proposed half a century ago (Gallardo, 1963) and whose

monophyly is corroborated in our results. The paraphyly

of Leptodactylus s.l. with respect to Hydrolaetare in our to-

tal evidence results owes to recent taxonomic changes to

the content of Leptodactylus and might, therefore, be bet-

ter addressed by reverting to the previous content.

Frost et al. (2006) placed Adenomera Steindachner,

1867, as a synonym of Lithodytes Fitzinger, 1843, and

Lithodytes as a subgenus of Leptodactylus noticing that

“Heyer (1998) and Kokubum and Giaretta (2005) also

presented evidence that recognizing Adenomera renders

Leptodactylus paraphyletic and that Lithodytes is the sis-

ter taxon of Adenomera.” However, this taxonomic ac-

tion was not required given that in Frost et al.’s (2006)

phylogeny none of the genera were rendered paraphy-

letic. Subsequent morphological analyses also suggested

the paraphyly of Leptodactylus relative to Adenomera and

Lithodytes (Ponssa 2008; Ponssa et al. 2010). However,

the reciprocal monophyly of Leptodactylus s.s., Adenomera

(= L. marmoratus group), and Lithodytes s.s. was supported

in other molecular studies (Pyron and Wiens, 2011; Fou-

quet et al. 2013), leading a recent study to conclude that

“proper sampling within Leptodactylus and Adenomera as

well as the integration of Hydrolaetare is still needed to

test the monophyly of these groups within Leptodactyli-

nae (Fouquet et al., 2013:447).”

The present analysis is the first to combine both the

molecular and non-molecular evidence, and it supports

the monophyly of the three groups. These three genera

and Hydrolaetare (Souza and Haddad, 2003; Fouquet

et al., 2013) all produce foam nests, but Adenomera dif-

fers from Leptodactylus s.s. in having facultative endotro-

phic larvae that complete their development in the nest,

whereas the others (except L. fallax and L. pentadactylus,

see below) have free-swimming larvae that leave the nest

after hatching (Altig and McDiarmid, 1999). As such,

based on our results, and in order to recognize the sepa-

rate evolutionary trajectory of this lineage based on life

history traits we remove Adenomera Steindachner, 1867

(type species: Adenomera marmorata Steindachner, 1867,

by monotypy) from the synonymy of Lithodytes and con-

sider it to be a genus corresponding to the clade currently

recognized as the L. marmoratus group.

Continued recognition of Hydrolaetare and resur-

rection of the genus Adenomera necessitate the recogni-

tion of Lithodytes at the generic level as well. Although

Lithodytes is currently monotypic, we based our decision

on: (1) the placement of Lithodytes as sister to Adenomera

(Fig. 3), (2) Lithodytes lacks endotrophic larvae (differen-

tiating it from its sister taxon Adenomera, (3) morpholo-

gy, and (4) the more than 6% divergence of the mitochon-

drial large ribosomal subunit between samples from Mato

Grosso, Brazil and Perú reported by Fouquet et al. (2007)

suggests that the widespread taxon Lithodytes lineatus

consists of at least two species. As such, we anticipate

that other species will soon be described given the pub-

lished evidence. We believe it better serves the needs of

working biologists and documentation efforts, taxonomic

understanding, and reconciling synonyms (Costello et al.,

2013) to recognize Adenomera and Hydrolaetare now than

to await the formal description of additional species of

Lithodytes. Therefore, herein we remove Lithodytes Fitz-

inger, 1843 as a subgenus of Leptodactylus and place it at

the genus rank.

Ingroup monophyly and relationships

The monophyly of Leptodactylus s.s. is well support-

ed (GB = 24). Due to the lack of morphological evidence

for Hydrolaetare, the sister group of Leptodactylus, no

non-molecular character-states optimize to this node un-

der accelerated transformation (Swofford and Maddison,

1992). Nevertheless, 15 phenotypic transformations oc-

cur at this node under delayed transformation (Table 1).

Assuming the current topology, some of these optimiza-

tions remain unaltered when available evidence from Hy-

drolaetare is considered. For example, Hydrolaetare lacks

nuptial excrescences on the thumb (Lynch, 1971; Souza

and Haddad, 2003), so the occurrence of two spines on

the thumb in adult males persists as a synapomorphy

of Leptodactylus. In contrast, both Leptodactylus and Hy-

drolaetare share a prominent posterior epiotic eminence

(Lynch, 1971), so this character-state originates at the

shared Hydrolaetare + Leptodactylus node.

Our results disagree with recently published hy-

potheses of the phylogeny of Leptodactylus. The analy-

ses of Ponssa (2008) and Ponssa et al. (2010) of adult

osteology recovered Leptodactylus discodactylus outside

Leptodactylus in a clade with Lithodytes and Adenomera.

Furthermore, those studies also recovered a sister clade

relationship between the L. latrans + L. melanonotus and

L. pentadactylus + L. fuscus clades. Those species group re-

lationships were previously suggested (Heyer, 1969b) and

supported by a study of larval internal anatomy based on




S12


Table 1. Non-molecular transformation events delimiting the major clades of Leptodactylus. All transformations are unambiguously optimized except

those reported for Leptodactylus, which are reported under delayed transformation optimization (see text for explanation).

Clade Character Ancestral State Derived State

Leptodactylus 12: Dark supratympanic stripe 0: Absent 2: Extending dorsad above tympanum

and continuing posterolaterad behind

the tympanum

21: Nuptial excrescences on thumb 3: Sandpaper-like nuptial callosities 2: Two lateral keratinized spines

43: Termination of pars facialis of

maxilla

0: Anterior to palatines 1: At level of palatines

49: Posterior termination of maxillary

teeth

0: Anterior to the anterior tip of the

quadratojugal

1: Reaching or surpassing the anterior

tip of the quadratojugal

52: Position of tectum nasi 1: At the same level as alary processes

of premaxillae

0: Posterior to alary processes of

premaxillae

59: Posterior epiotic eminence 0: Part of the overall shape of the otic

capsule, lacking a posterolateral

extension beyond the otic capsule

body

1: prominent, extending laterally

beyond the otic capsule body

71: Anterior expansion of nasals 0: Absent 1: Present, anterior apex forming a

distinct protuberance

76: Vomerine teeth 0: Arranged in a straight line 1: Arranged in a shallowly arched series

78: Number of vomerine teeth 1: 2–7 2: > 8

84: Ridge on ventral surface of palatine 0: Absent 1: Present, superficial and hardly

noticeable

87: Anterior extension of anterior

ramus of pterygoid

1: Contacting palatine 0: Not reaching palatine

94: Anteromedial process of hyoid 1: Present 0: Absent

96: Depth of hyoglossal sinus 1: Reaching anterior borders of alary

processes

2: Deep, extending 2 mm past anterior

borders of the alary process

102: Neural spine of vertebrae I–V 1: Non-imbricate 2: Imbricate

145: Parental care 0: Absent 1: Present, care of nest

L. fuscus group 18: Toe webbing 1: Present as weak basal fringe and/or

web

0: Absent

64: Nasals 1: Adjacent or in medial contact along

the middle or anterior portion

2: Adjacent or in medial contact along

entire length

L. pentadactylus

group + L. latrans

group + L. melanonotus

group

64: Nasals 1: Adjacent or in medial contact along

the middle or anterior portion

0: Separated

104: Position of base of occipital

condyles relative to posterior-most

points of the skull

0: Posterior 1: Anterior

145: Parental care 1: Present, care of nest 2: Present, care of nest and larvae

L. pentadactylus group 24: Male chest spines 0: Absent 1: Present

31: Inguinal gland 0: Absent 1: Present

96: Depth of hyoglossal sinus 2: Deep, extending 2 mm past anterior

borders of the alary processes

3: Very deep, extending > 2 mm past

anterior borders of alary processes

L. latrans group +

L. melanonotus group

18: Toe webbing 1: Present as weak basal fringe and/or

web

2: Present, fringes extending along

entire length of the toes except tips

113: Relationship between suprarostral

corpus and ala

1: Fused dorsally 2: Fused ventrally

116: Planum trabeculare anticum width 0: Wide 1: Narrow

122: Attachment of processus ascendens 1: Intermediate 0: Low

129: Processus branchialis 0: Open 1: Closed

L. latrans group 16: Color patter of ventral surface of

thighs

1: Pigmented, different patterns

evident on entire surface: uniformly

pigmented, labyrinthine, vermiculate,

spotted

0: Immaculate or with spots on the

margins

36: Keratinized male tarsal fold 0: Absent 1: Present

109: Shape of terminal phalanges 1: Rounded and bifurcated: dilated with

a split that defines two lobules

0: Rounded or knobbed

L. melanonotus group 40: Angle between mentomeckelian

and angulosplenial

1: Approximately parallel 0: Acute

52: Position of tectum nasi 0: Posterior to alary processes of

premaxillae

1: At the same level as alary processes

of premaxillae

91: Skull proportions 0: Wider than long 1: Width and length subequal or longer

than wide

121: Processus posterolateralis of crista

parotica

0: Distinct 1: Reduced

130: Hyoquadrate process 0: Small, triangular 1: Large, rounded




S13


the analysis of 22 species of Leptodactylus (Larson and de

Sá, 1998). A histological study of tadpole buccal foam-pro-

ducing glands of Adenomera sp. and two species of Lepto-

dactylus (L. furnarius and L. labyrinthicus) by Giaretta et al.

(2011) suggested two characters that were mapped, along

with seven other reproductive traits, on Ponssa et al.’s

(2010)1 phylogeny. This study lacks rigorous ingroup and

outgroup sampling to place their findings in an evolution-

ary framework. Subsequently, Fouquet et al.’s (2013) phy-

logenetic analysis of foam-nest building showed that tad-

pole buccal foam-producing glands are homoplasic traits

in Adenomera and the Leptodactylus fuscus species group.

Consequently, herein we reject Giaretta et al.’s (2011)

proposed use of the name Spumoranuncula to cluster spe-

cies of Adenomera with the L. fuscus and L. pentadactylus

species groups. Miranda et al. (2014) proposed a phylo-

genetic hypothesis based on larval characters of 22 Lepto-

dactylus species built on previous studies (Larson and de

Sá, 1998; de Sá et al., 2007a, b) and coded chondrocranial

data for four species (L. camaquara, L. spixi, L. troglodytes,

and L. furnarius, although the chondrocranial morpholo-

gy was not reported) and internal oral anatomy of larvae.

Among recognized species groups, Miranda et al. (2014)

recovered only the L. latrans group as monophyletic. Lep-

todactylus riveroi was recovered as the sister taxon of the

remainder of the genus, which results in a polyphyletic

L. melanonotus group. Furthermore, the L. latrans and

most of the L. melanonotus species groups were imbedded

within the L. fuscus group. Finally, L. rhodomystax, a mem-

ber of the L. pentadactylus species group, was sister taxa

to the all other Leptodactylus except L. riveroi. The low

resolution of the tree based on larval characters (Miranda

et al., 2014:6, fig. 4) could be due to the low number of

taxa included in the analyses and the high level of homo-

plasy of larval internal oral anatomy characters (reported

previously by Wassersug and Heyer, 1988) as a result of

anuran larval caenogensis. However, the trees resulting

from the combination of larval and non-molecular adult

characters (although different sampling of taxa was uti-

lized) also exhibit poor resolution of Leptodactylus rela-

tionships (Miranda et al., 2014:7, fig. 5).

At the same time, our results generally support the

species groups proposed by Heyer (1969b). Although

those groups are not strictly monophyletic, exceptions

involve only a few species that are easily accommodated

without proposing new groups or significantly changing

their contents (see below). The four groups form a pec-

tinate tree, with the Leptodactylus fuscus group diverging

first, followed by the L. pentadactylus group, which is sis-

ter to the L. latrans and L. melanonotus groups (Fig. 3B).

The clade formed by the Leptodactylus pentadac-

tylus, L. latrans, and L. melanonotus groups has not

1 Giaretta et al. (2011) refer to Ponssa et al. (2008), but there is no such

publication.

been proposed previously. Support for the clade is weak

(GB = 5), but the clade is diagnosed by three unambigu-

ously optimized transformations, two from osteology and

one from behavior (Table 1).

The clade formed by the Leptodactylus latrans and

L. melanonotus groups is well supported (GB = 18) and

was recognized previously on the basis of five synapo-

morphies in the larval chondrocranium (Larson and de

Sá, 1998). Among those synapomorphies, a closed pro-

cessus branchialis between ceratobranchials II and III is

a synapomorphy distinguishing species of the L. latrans

group + L. melanonotus clade from all other Leptodactylus.

More recently, an analysis of osteological data to assess

the relationships of L. nesiotus agreed with the previous

study and added two more synapomorphies for this clade

(Ponssa et al., 2010). In the present analysis, this clade is

delimited by five unambiguously optimized transforma-

tions. Beyond the molecular evidence and morphological

characters noted above that support the monophyly of

the L. latrans + L. melanonotus clade, the group is unique

in the elaborate complex social larval and parental care

behaviors that have evolved in this clade.

Leptodactylus fuscus group

We found the traditionally defined Leptodactylus

fuscus group to be monophyletic. However, we also found

two species of the traditionally defined L. pentadactylus

group, L. laticeps and L. syphax, to be sister to the L. fus-

cus group, thereby rendering the L. pentadactylus group

paraphyletic. Consequently, we transfer L. laticeps and

L. syphax to the L. fuscus group, thereby rendering both

the L. fuscus and L. pentadactylus groups monophyletic

(see below). This expanded L. fuscus group is well sup-

ported (GB = 16; Fig. 3B) and is diagnosed by two un-

ambiguously optimized non-molecular transformations

(Table 1). Within the L. fuscus group, we recovered a clade

consisting of L. ventrimaculatus and L. labrosus, which

form the sister clade to all other species of the L. fuscus

group. Next, L. bufonius is recovered basal in a clade that

also include L. troglodytes and L. mystacinus as sister taxa;

these three species are the sister clade to the remaining

species in the L. fuscus group.

Although they did not explicitly identify any diag-

nostic character-states, Heyer et al. (1996a) analyzed the

advertisement calls of a group of similar species they re-

ferred to as the Leptodactylus mystaceus species complex

(L. mystaceus, L. spixi, L. notoaktites, L. elenae, and L. didy-

mus). Caramaschi et al. (2008) described L. cupreus as per-

taining to this complex and Cassini et al. (2013) suggested

that L. cupreus is closely related to L. mystacinus; our evi-

dence does not support the inclusion of L. mystacinus in

the L. mystaceus species complex.

Species identification within the Leptodactylus

mystaceus species complex remains problematic and




S14


challenging. Leptodactylus didymus and L. mystaceus are

morphologically indistinguishable and recognizable only

by characteristics of their advertisement calls: non-pulsed

in L. didymus and pulsed in L. mystaceus (Heyer et al.,

1996a). Nevertheless, our evidence placed L. didymus as

sister to the remainder of the L. mystaceus species com-

plex, thereby supporting a previous study (de Sá et al.,

2005b) based on fewer species that indicated that L. did-

ymus and L. mystaceus were not sibling species (sensu

Mayr, 1942). Similarly, L. mystaceus was not monophylet-

ic in our analysis, with one sample recovered as sister to

a clade that includes L. notoaktites and two other samples

of L. mystaceus, which are the sister group of four L. fuscus

samples. This suggests that the nominal L. mystaceus in-

cludes undescribed cryptic species.

Fouquet et al. (2007) recovered Leptodactylus longi-

rostris embedded within L. fuscus. In our results, L. longi-

rostris is sister to L. poecilochilus within a clade that also

includes L. fragilis, and that clade forms the sister group

to a clade of five additional L. fuscus samples. Our finding

that L. fuscus is non-monophyletic is in overall agreement

with the previous identification of three geographical lin-

eages within L. fuscus (Camargo et al., 2006).

Although Leptodactylus plaumanni and L. gracilis have

been considered a classical example of morphological sib-

ling species in Leptodactylus recognized only by their ad-

vertisement calls (Heyer, 1978; Cardoso, 1985), our find-

ings reveal that their phylogenetic affinities are actually

quite distant. Leptodactylus plaumanni and L. marambaiae

clade are the sister clade to L. cunicularius, L. furnarius,

and L. camaquara; L. tapiti is the sister taxa to these two

clades. In contrast, L. gracilis is nested within a clade with

a basal L. latinasus and the sister species L. sertanejo and

L. joyli.

Leptodactylus pentadactylus group

As noted above, we transferred two traditionally

Leptodactylus pentadactylus group species (L. laticeps and

L. syphax) to the L. fuscus group. Further, we found that

L. lithonaetes, a species previously not assigned to any

species group (Heyer, 1995), is recovered within the

L. pentadactylus group and as sister to a clade that in-

cludes L. rugosus and the sister pair of L. rhodonotus and

L. rhodomystax. This four-species clade is sister to the re-

mainder of the L. pentadactylus group. Consequently, we

transfer L. lithonaetes to the L. pentadactylus group, which

is delimited by two externally visible character-states

(presence of chest spines in males; presence of a conspicu-

ous inguinal gland) and one from internal anatomy (very

deep hyoglossal sinus) and has GB = 8 (Table 1, Fig. 3B).

Our results show that Leptodactylus labyrinthicus is

sister to L. fallax within a clade that also includes L. knud-

seni, whereas L. paraensis and L. vastus, the latter recog-

nized as distinct from L. labyrinthicus by Heyer (2005),

are recovered as sister taxa that are not closely related to

L. labyrinthicus. Recently, Jansen and Shulze (2012) re-

ported that Bolivian populations identified previously as

L. labyrinthicus (e.g., De la Riva et al., 2000) are genetically

similar to L. vastus and L. paraensis; those authors tenta-

tively assigned the Bolivian populations to L. vastus, re-

porting red coloration of the thighs and groin of Bolivian

specimens. The same coloration is found in juvenile–sub-

adult specimens of L. vastus from Brazil (see Plate 8E).

Red coloration on the groin and posterior and anterior

surfaces of the thighs is common in juvenile stages of

species in the L. pentadactylus species group (e.g., L. laby-

rinthicus, Plates 6C–D; L. myersi, Plate 6E; L. peritoaktites,

Plate 7B). The striking difference in coloration between

juveniles and adults is unknown in other Leptodactylus

species groups and, therefore, might be an additional sy-

napomorphy for the L. pentadactylus group. Jansen and

Shulze (2012) also noted that Heyer (2005) reported ex-

tensive intraspecific variation in morphological charac-

ters but did not provide unique diagnostic characters for

species identification to differentiate the newly described

species.

Our analysis recovered Leptodactylus myersi as sis-

ter of a clade consisting of L. peritoaktites and the sister

species L. pentadactylus and L. savagei. Heyer (2005) rec-

ognized L. peritoaktites and L. savagei as distinct from

L. pentadactylus based on evidence from morphology and

vocalizations. In life, juveniles of L. peritoaktites have

distinct bright red coloration on thighs and groin (RdS,

pers. obs.); this coloration has not been reported for ju-

veniles of either L. pentadactylus or L. savagei. Recently, a

closer relationship between L. savagei and L. pentadactylus

was suggested (Jansen and Shulze, 2012); however, in that

analysis the relationships of L. rhodomerus were uncertain

and L. peritoaktites and L. myersi were not included.

Leptodactylus latrans group

Our evidence corroborated the monophyly of the

Leptodactylus latrans group, with L. silvanimbus placed as

sister to all other species in the group (Fig. 3B). Leptodac-

tylus silvanimbus is unique among Leptodactylus in that it

is restricted to relatively high elevations (1,700–1,900 m)

and has 24 chromosomes (Amaro-Ghilardi et al., 2006; all

other known Leptodactylus have at most 2n = 22; 2n = 20–

22 in L. podicipinus, Gazoni et al., 2012). This species was

first placed in the L. pentadactylus species group (McCra-

nie et al., 1980) and was then transferred to the L. mela-

nonotus species group based on external larval morphol-

ogy (McCranie et al., 1986) and call characteristics (Heyer

et al., 1996b). On the basis of their analysis of morpholog-

ical and limited molecular evidence, Heyer et al. (2005a)

rejected the association of L. silvanimbus with the L. mela-

nonotus group and suggested a possible basal position

of the species in the genus, but they did not associate it




S15


with any of the Leptodactylus species groups. Leptodacty-

lus silvanimbus was recovered nested within Leptodactylus

in a polytomy with L. melanonotus and a clade consisting

of L. riveroi, L. discodactylus, and L. diedrus by de Sá et al.

(2005a). Given its phylogenetic position in our results, we

transfer L. silvanimbus to the L. latrans group and inter-

pret its unique chromosome number as autoapomorphic.

This expanded L. latrans group is delimited by three un-

ambiguous non-molecular transformations (Table 1) and

has a GB value of 16 (Fig. 3B).

The clade formed by Leptodactylus bolivianus and

L. insularum is the sister group to the remaining species

in the L. latrans species group. Recently, a third species—

L. guianensis—was described from this species complex

(Heyer and de Sá, 2011). This species was not included

in our analyses, but according to the original description

it is more closely related to L. bolivianus (adult males with

single thumb spine in both species) than to L. insularum

(adult males with two thumb spines).

Leptodactylus viridis was first placed in the L. melano-

notus species group by Jim and Spirandeli Cruz (1973) but

was transferred to the L. latrans species group by Heyer

and Maxson (1982). We recovered L. viridis imbedded in

the L. latrans group and sister to the L. latrans–L. macro-

sternum species complex. Within this species complex,

it is interesting to note that L. chaquensis is more closely

related to L. macrosternum than to L. latrans, although

L. chaquensis and L. latrans have been considered sib-

ling species since L. chaquensis was described (Cei, 1950,

1962).

Leptodactylus melanonotus group

Our results show that Leptodactylus riveroi, a species

not strongly associated with any species group previously,

is part of the L. melanonotus group. It is recovered as sister

to L. melanonotus, which together are sister to all other

L. melanonotus group species. This result is consistent

with previous results by de Sá et al. (2005a) that report-

ed L. riveroi to be sister to a clade composed of L. diedrus

and Vanzolinius (= L. discodactylus). The relationships of

L. riveroi have been unclear since its original description

suggested that it was morphologically intermediate be-

tween the L. latrans and L. melanonotus species groups

(Heyer and Pyburn, 1983). Although we find L. riveroi to

be nested within the L. melanonotus group, its relatively

basal position is consistent with previous suggestions by

Heyer and Pyburn (1983) and Larson and de Sá (1998).

The L. melanonotus group (including L. riveroi) is delim-

ited by five unambiguous non-molecular transformations

(Table 1) and has a GB value of 25 (Fig. 3B).

Leptodactylus colombiensis and L. wagneri are sister

taxa in a clade with L. validus. This clade is sister to all

remaining taxa in the melanonotus species clade. Our re-

sults corroborate previous findings that L. discodactylus

is nested within Leptodactylus (de Sá et al. 2005a; Frost

et al. 2006) and, therefore, that its recognition as the

monotypic genus Vanzolinius would render Leptodactylus

paraphyletic. Our data decisively place this species within

the L. melanonotus group, as originally suggested by Heyer

(1970a), although he hypothesized L. discodactylus to be

sister to all other species of the group. Instead, we found

L. discodactylus to be sister to L. griseigularis (GB = 10)

and that clade to be sister to L. podicipinus + L. diedrus.

The remaining species of the L. melanonotus group form

a clade consisting of L. nesiotus as sister to two pairs of

species, L. leptodactyloides + L. petersii and L. natalensis +

L. pustulatus.

The relevance of non-molecular evidence

By the end of the 20th century, modern systematics,

aided by technological advancements such as Sanger se-

quencing and PCR technology (Sanger et al. 1977; Mul-

lis, 1990), had become dominated by DNA sequence data.

Undoubtedly, this owes largely to the ease and decreas-

ing cost with which large data sets could be assembled—a

situation that promises to improve even more with next

generation of sequencing methods. In contrast, scoring

morphological characters requires time-consuming study

to obtain specialized knowledge that ultimately returns

only a fraction of the amount of evidence provided by mo-

lecular data. In light of this situation, the question faced

by practically minded professional scientists, graduate

students in training, undergraduates, and funding agen-

cies alike is whether or not it is worthwhile to dedicate the

months or even years necessary to obtain a comparatively

small number of morphological characters instead of se-

quencing more loci. That is, in terms of biological knowl-

edge, understanding the evolution of the phenotype is at

least as intrinsically important as understanding the evo-

lution of the genotype (Love, 2003; Wake et al., 2011),

and epistemologically the increased explanatory power

that results from including additional evidence validates

total evidence analysis (Grant and Kluge, 2003; Kluge,

2004). However, in practical terms, do non-molecular

characters matter?

To evaluate the effect of the non-molecular evidence

on our results, we repeated the analyses using only the

molecular evidence. Assuming that truly optimal trees

were obtained in both heuristic searches, any differences

between the results of the two analyses must be due to

the morphological evidence. Given our taxon and charac-

ter sampling, we focus these comparisons on the relation-

ships within Leptodactylus.

Analysis of the molecular-only dataset resulted in 12

most parsimonious trees of 15,472 steps (Fig. 4). Good-

man-Bremer values were calculated using the 573,183

trees visited during the TBR swap of one of the optimal




S16


Leptodactylus fragilis

Leptodactylus melanonotus

Hydrolaetare dantasi

Hydrolaetare caparu

Leptodactylus ventrimaculatus

Leptodactylus labrosus

Leptodactylus syphax

Leptodactylus laticeps

Leptodactylus latinasus

Leptodactylus gracilis

Leptodactylus sertanejo

Leptodactylus joyli

Leptodactylus tapiti

Leptodactylus plaumanni

Leptodactylus marambaiae

Leptodactylus cunicularis

Leptodactylus furnarius

Leptodactylus camaquara

Leptodactylus albilabris

Leptodactylus poecilochilus

Leptodactylus longirostris

Leptodactylus fuscus





Leptodactylus bufonius

Leptodactylus troglodytes

Leptodactylus mystacinus

Leptodactylus elenae

Leptodactylus mystaceus

Leptodactylus didymus

Leptodactylus notoaktites







Leptodactylus lithonaetes

Leptodactylus rugosus

Leptodactylus rhodonotus

Leptodactylus rhodomystax

Leptodactylus flavopictus

Leptodactylus stenodema

Leptodactylus vastus

Leptodactylus paraensis

Leptodactylus peritoaktites

Leptodactylus savagei

Leptodactylus pentadactylus

Leptodactylus myersi

Leptodactylus labyrinthicus



Leptodactylus knudseni

Leptodactylus fallax

Leptodactylus silvanimbus

Leptodactylus insularum

Leptodactylus bolivianus

Leptodactylus viridis

Leptodactylus latrans



Leptodactylus chaquensis

Leptodactylus macrosternum


Leptodactylus riveroi

Leptodactylus wagneri

Leptodactylus colombiensis

Leptodactylus validus continetal

Leptodactylus validus



Leptodactylus nesiotus

Leptodactylus pustulatus

Leptodactylus natalenis

Leptodactylus petersii

Leptodactylus leptodactyloides

Leptodactylus grisegularis

Leptodactylus discodactylus

Leptodactylus podicipinus

Leptodactylus diedrus


1

2

3

4

5

1

2

3

6

7

8

9

1

2

3

2

NEOTYPE

1

1

2

1

2

3

sp

15

7.9

7.9

7.9

7.9

7.9

17

9.0

11

8

6

13

20

11

11

19

10

6

3.2

3.2

3.2

3.2

2

1.1

1.1

1.1

1.1

4

2.1

2.1

2.1

2.1

14

7.4

7.4

9

4.8

4.8

4.8

4.8

14

6

20

43

23

26

14

34

18

4

1

15

13

6.9

6.9

12

8

4.2 4.2

4.2

4.2

4.2

4.2

7

22

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1

8

14

7.4

17

9.0

15

32

17

8

12

4

9

11

11

1

8

2

27

14

10

5.3

5.3

5.3

5.3

5.3

11

41

14

7.4

7.4

14

2

9

10

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12

10

10

10

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1

18

9.5

5

2.6

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8

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1

0.5

0.5

0.5

0.5

0.5

0.5

0.5

0.5

11

5.8

5.8

5.8

5.8

5.8

3

1.6

1

1

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6.3

6.3

6.3

6.3

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7

3.7

3.7

3.7

23

12

41

22

22

15

64

34

Figure 4. Strict consensus of 12 most parsimonious trees (15,472 steps) from the molecular-only analysis. Values below branches are Goodman-Bremer

support and above branches are REP support. Terminals coded for non-molecular characters are marked with an asterisk (*). Red = L. fuscus species group,

green = L. pentadactylus species group, orange = L. latrans species group, blue = L. melanonotus species group.




S17


trees. The least parsimonious tree was 34,404 steps.

Within Leptodactylus, relationships in the two analyses

are largely congruent, and the pairwise rooted SPR dis-

tances between the most parsimonious trees with and

without morphology are only 23–25 SPR moves (for

comparison, the distances between equally parsimonious

trees from the same dataset are only 1–3 SPR moves). Ex-

tensive congruence between the topologies is not surpris-

ing given that the total evidence dataset is dominated by

molecular evidence.

Nevertheless, comparison of REP values within

Leptodactylus from the two analyses (Figs. 3B, 4) demon-

strates that support for most clades increased with the in-

clusion of morphological evidence (mean REP for total ev-

idence dataset = 6.7; mean REP for molecular-only dataset

= 6.3; Hydrolaetare not included, see below). For example,

REP support for Leptodactylus (including Hydrolaetare)

was 7.9 in the molecular-only analysis and increased to 12

in the total evidence analysis. Among the 54 clades that

are shared between the two strict consensus topologies,

REP increased for 30 clades (56%), remained the same

for eight clades (15%), and decreased for 16 clades (30%).

For example, REP support for the L. latrans group, which

was monophyletic in both analyses, increased from 6.9 in

the molecular-only analysis to 8.2 with the inclusion of

morphological evidence. Within the L. fuscus group, the

L. ventrimaculatus + L. labrosus clade is one of the most

strongly supported relationships in both analyses; how-

ever, although GB support increased from 41 in the mo-

lecular-only analysis to 42 in the total evidence analysis,

REP was 22 in both analyses, indicating that the increase

in support merely kept pace with the overall increase in

evidence in the total evidence analysis (Grant and Kluge,

2009). Also within the L. fuscus group, the monophyly of

L. poecilochilus and L. longirostris was supported in both

analyses, but REP decreased from 7.9 in the molecular-

only analysis to 5.7 in the total evidence analysis.

The only species group that is monophyletic with-

out non-molecular evidence is the Leptodactylus latrans

group, and the topology of the group is also identical in

the two analyses. The monophyly of the L. fuscus group

is violated by the placement of L. fragilis as the sister of

all other species of Leptodactylus. Within the L. fuscus

group, L. bufonius, L. troglodytes, and L. mystacinus form

a clade near the root of the group in the total evidence

results, but they form a grade that is deeply nested within

the L. fuscus group in the molecular-only analysis. In con-

trast, L. didymus, L. mystaceus, and L. elenae form a grade

in the total evidence analysis but are monophyletic in the

molecular-only analysis.

The Leptodactylus pentadactylus group is paraphy-

letic in the molecular-only analysis, with most of the

group being more closely related to most of the L. melano-

notus group than to L. lithonaetes, L. rugosus, L. rhodono-

tus, and L. rhodomystax. Leptodactylus myersi is sister to

L. labyrinthicus, Leptodactylus knudseni, and L. fallax in the

molecular-only analysis, but is sister to L. peritoaktites,

L. savagei, and L. pentadactylus in the total evidence analy-

sis. Similarly, L. knudseni and L. fallax are sister species in

the molecular-only results, whereas in the total evidence

results L. knudseni is sister to L. fallax and L. labyrinthicus.

Most of the relationships within the Leptodacty-

lus melanonotus group are identical in the two analyses.

However, in the molecular-only results L. melanonotus

is placed near the base of Leptodactylus as the sister of

Hydrolaetare, which is sister to Leptodactylus in the total

evidence results but is placed within Leptodactylus in the

molecular-only results. The different placement of Hy-

drolaetare in the two analyses was unexpected because

neither species of that clade was scored for any non-mo-

lecular characters. However, although this result might

seem counter-intuitive, it is easily explained and reveals

a previously under-appreciated effect of adding even a

comparatively small amount of morphology (or any other

class of evidence) to a subset of the terminals in a dataset:

the inclusion of morphology for a subset of terminals al-

ters the optimal position of those terminals and, in doing

so, also alters the respective molecular character optimi-

zations, which alters the optimal placement of terminals

for which morphology was not added. In the present case,

the morphological characters made it more parsimonious

for L. melanonotus to be placed with other species of the

L. melanonotus group, L. fragilis to be placed with other

species of the L. fuscus group, and the two clades of the

L. pentadactylus group to be placed as sisters, all of which

changed the molecular optimizations such that Hydrola-

etare is optimally placed outside Leptodactylus.

In conclusion, even though non-molecular evidence

comprises only 3.5% of the total evidence matrix (4,263

aligned nucleotides, 156 morphological characters), our

results showed unequivocally that non-molecular evi-

dence had a strong impact on our results. The distance

between optimal topologies from the two analyses was

23–25 rooted SPR moves. Among the 54 Leptodactylus

clades that are shared by the two analyses, support dif-

fered in 85% when non-molecular evidence was included,

increasing in 56% and decreasing in 30%. More impor-

tantly, although monophyly of all four of the tradition-

ally recognized species groups required only minor rear-

rangements of a few species in the total evidence analysis,

only one species group was monophyletic in the molecu-

lar-only analysis, with no way of rearranging species to

resemble the other groups. Finally, analysis of only DNA

sequences without non-molecular data resulted in the

inclusion of Hydrolaetare within Leptodactylus, whereas

analysis of the combined molecular and non-molecular

dataset placed Hydrolaetare outside Leptodactylus, even

though no morphological evidence was coded for Hydro-

laetare. Clearly, non-molecular evidence mattered in the

present study.




S18


Evolution of Leptodactylus traits

In addition to elucidating the pattern of phyloge-

netic diversification of Leptodactylus, our results have

implications for the evolution of several aspects of their

natural history. Below we discuss the invasion of rocky

outcrops, construction of foam nests, parental care, and

larval oophagy.

Invasion of rocky outcrops

Species of Leptodactylus inhabit a variety of habi-

tats, but only three species of the L. pentadactylus species

group (viz., L. lithonaetes, L. rugosus, and L. myersi) and

one of the L. fuscus species group (viz., L. syphax) inhabit

and are restricted to rocky outcrops. Based on our phylog-

eny, speciation related to the invasion and apparent adap-

tation to this unique habitat occurred three or four times

in the evolutionary history of Leptodactylus, depending

on whether the ancestor of the L. lithonaetes, L. rugosus,

L. rhodonotus, and L. rhodomystax clade in the L. pentadac-

tylus group inhabited rocky outcrops or not (both possi-

bilities are equally parsimonious; Fig. 5). The geographic

distribution of these rocky outcrop species was modeled

and areas that need to be surveyed for the likelihood of

occurrence of these, or of yet undescribed, species were

identified by Fernández et al. (2009).

Foam nest construction

Construction of foam nests is widespread in Lepto-

dactylidae and some other anuran clades (Faivovich et al.,

2012; Fouquet et al., 2013) and enhances the survival of lar-

vae by providing protection against desiccation and at least

some predators (Vaz Ferreira and Gehrau, 1975; Downie,

1996). In Leptodactylus, the foam nests result from the am-

plectic pair—but mostly the male—beating with their hind

limbs the oviductal secretions released during oviposition

(Gallardo 1958, 1964a). A recent study suggested that foam

nest construction in Leptodactylidae either evolved once

and was subsequently lost in the genus Pseudopaludicola or

evolved independently in Leptodactylinae and Leiuperinae

(Fouquet et al., 2013). Our results confirm that foam nest

construction is plesiomorphic in Leptodactylus.

Heyer (1969b) surmised that the genus exhibited a

tendency to terrestriality with the Leptodactylus latrans

group + L. melanonotus group clade having the most

primitive reproductive modes of depositing a foam nest

on the surface of water and having exotrophic larvae. The

implicit idea of a ‘progression’ towards terrestriality was

subsequently embraced by other authors (e.g., Duellman,

1985; Prado et al., 2002). However, our results suggest a

more complex evolutionary history of these traits.

In Leptodactylus the placement of foam nests in un-

derground chambers is restricted to the L. fuscus group

and L. fallax and L. vastus (in the latter species suggested,

but unconfirmed; see below) of the L. pentadactylus group,

with other species characterized by aquatic foam nests.

Based on our optimal topology, the occurrence of ter-

restrial foam nests is unambiguously and independently

derived in L. fallax and L. vastus (if confirmed), because

the remainder of the L. pentadactylus group possesses

aquatic foam nests. However, due to the distribution of

aquatic and terrestrial foam nests in close relatives—

terrestrial in Adenomera (Haddad and Prado, 2005) and

probably also in Lithodytes (Lamar and Wild, 1995), po-

tentially aquatic or terrestrial in Hydrolaetare (Souza and

Haddad, 2003)—the ancestral state for Leptodactylus is

ambiguous. If foam nests in Hydrolaetare are found to be

terrestrial, then the terrestrial foam nests of the L. fuscus

group are plesiomorphic and the aquatic foam nests of the

L. pentadactylus, L. latrans, and L. melanonotus groups are

a synapomorphic; alternatively, if Hydrolaetare has aquat-

ic foam nests, then the ancestral state for Leptodactylus

will remain ambiguous.

Previous studies have also concluded that the evo-

lution of foam nests is more complex than the precon-

ceived notions of linear, progressive, evolutionary trends

(Faivovich et al., 2012; Fouquet et al., 2013), and quan-

titative studies of other previously assumed progressive

scenarios have arrived at similar conclusions. For exam-

ple, the aquatic, nocturnal species Aromobates nocturnus

is not the plesiomorphic sister species of all other den-

drobatids (Myers et al., 1991) but is instead deeply nested

within an otherwise terrestrial, diurnal clade (Grant et al.,

2006). Perhaps more dramatically, in both plethodontid

salamanders (Chippindale et al., 2004; Chippindale and

Wiens, 2005) and Gastrotheca (Wassersug and Duellman,

1984; Wiens et al., 2007) some biphasic species appear

to have evolved from direct-developing ancestors that, in

turn, evolved from biphasic ancestors.

Although the larvae of Leptodactylus laticeps (L. fus-

cus group) and L. myersi (L. pentadactylus group) remain

unknown, it would not be surprising for these larvae to

develop partially or completely underground; L. bufonius

(Schalk, 2012) and L. laticeps (Cei, 1980) were reported

to inhabit the underground caves of Lagostomus maximus

(Rodentia, Chinchillidae). Based on the phylogeny and

considering that L. myersi is restricted to rocky outcrops,

it is possible that L. myersi larvae are oophagous and de-

velop in underground burrows.

Placement of foam nests varies within other clades

from being placed on the surface of water bodies to be-

ing located in basins, either natural or excavated by the

male, at variable distances from the edges of ponds. Fur-

thermore, the larvae of L. pentadactylus (and likely associ-

ated species L. savagei, and L. peritoaktites) may or may

not complete development in the foam nest as a mecha-

nism to cope with unfavorable environmental conditions

(see below). It does not seem that the L. latrans group +




S19


L. melanonotus group clade has a primitive reproductive

mode but one that is characterized by highly specialized

and elaborate parental care. The complex behaviors found

in the L. latrans + L. melanonotus clade extend beyond con-

struction of a foam nests and involve elaborate behaviors

and interactions between adults and larvae.

Parental care

Eggs attended by at least one of the parents have nu-

merous benefits (reviewed by Crump, 1995). The earliest

reports available are for Leptodactylus latrans (Fernández

and Fernández, 1921; Gallardo, 1964b, 1970), which is

also the species that has been most studied. Vaz-Ferreira

and Gehrau (1974, 1975) provided the most complete

description of the complex behavior in L. latrans. These

authors documented that: (1) the foam nest is shaped like

a ‘crown’ or ‘ring’ of foam with a central hole where the

female sits; (2) females can leave and re-enter the foam

nest through underwater tunnels without disturbing the

nests; (3) mostly females, but also males in recently built

nests, actively protect the nest against predators with ag-

gressive behaviors that include jumping, biting, and emit-

ting a unique defensive call; (4) after hatching tadpoles

Leptodactylus latrans + L. melanonotus species groups

Leptodactylus syphax

Leptodactylus laticeps

Leptodactylus ventrimaculatus

Leptodactylus labrosus

Leptodactylus bufonius

Leptodactylus troglodytes

Leptodactylus mystacinus

Leptodactylus albilabris

Leptodactylus fragilis

Leptodactylus poecilochilus

Leptodactylus longirostris


Leptodactylus latinasus

Leptodactylus gracilis

Leptodactylus sertanejo

Leptodactylus joyli

Leptodactylus tapiti

Leptodactylus plaumanni

Leptodactylus marambaiae

Leptodactylus cunicularis

Leptodactylus furnarius

Leptodactylus camaquara

Leptodactylus didymus


Leptodactylus elenae

Leptodactylus notoaktites




Leptodactylus lithonaetes

Leptodactylus rugosus

Leptodactylus rhodonotus

Leptodactylus rhodomystax

Leptodactylus flavopictus

Leptodactylus stenodema

Leptodactylus vastus

Leptodactylus paraensis

Leptodactylus myersi

Leptodactylus peritoaktites

Leptodactylus savagei

Leptodactylus pentadactylus

Leptodactylus knudseni

Leptodactylus fallax


1

2

3

Figure 5. Distribution of some natural history traits reported in Leptodactylus. Optimizations are ambiguous due to extensive missing data; states

marked on internal nodes are unambiguously present in the respective hypothetical ancestors (although the state might have originated earlier) and are

known to occur in all descendant terminals. See text for details. Blue dot = occupation of rocky outcrops; yellow dot = facultative oophagous larvae; orange

dot = obligate oophagous larvae.




S20


form a school that moves together as a relatively compact

mass until metamorphosis; (5) females attend and ac-

tively protect the tadpoles; (6) tadpoles use their mouths

to scrape the dorsal surfaces of the female; (7) frequently

the females ‘push’ the mass of tadpoles toward the edge

of the ponds; (8) females rapidly raise the sacral region,

producing waves over the water surface; and (9) emission

of sounds is correlated with water surface waves produced

by the tadpoles and the attending female.

At least part of the complex behavior reported for

Leptodactylus latrans has been reported subsequently

for other species in the L. latrans group + L. melanonotus

group clade. Foam nests with adults (female or male) sit-

ting in its center and attending the eggs were reported

in L. chaquensis (Prado et al., 2000). A recent analysis of

the L. bolivianus species complex recognized L. guianensis

(Heyer and de Sá, 2011). Although not yet reported in the

literature, based on our phylogeny is it likely that L. guia-

nensis, L. macrosternum, and L. viridis also have ring shaped

nests and adults with similar behavioral patterns. Larval

schooling and parental attendance of eggs and larvae

have been reported in all species in the L. latrans species

group (L. latrans, Vaz-Ferreira and Gehrau, 1974; L. insu-

larum, Wells and Bard, 1988; L. macrosternum, Caldwell,

1992; L. bolivianus, Vaira, 1997; L. chaquensis, Prado et al.,

2000; Martins, 2001; Ponssa, 2001), except the recently

described L. guianensis, L. viridis (larvae unknown in both

species), and L. silvanimbus. Herein, we add L. silvanimbus

to the species with larval schooling. During fieldwork in

Honduras, one of us (RdS) observed a school of tadpoles

of this species moving through the water column as a ball

and rolling on top of each other while an adult remained

in close proximity; larvae from this school were used in

the larval description of the species (Heyer et al., 2002).

Larval schooling has also been reported for L. riveroi and

L. validus (Downie, 1996), L. leptodactyloides (Downie,

1996; Rodrigues et al., 2011), L. podicipinus (Prado et al.,

2000; Martins, 2001), L. melanonotus (Hoffman, 2006),

L. natalensis (Santos and Amorim, 2006), and L. pustu-

latus (de Sá et al., 2007a). Based on our phylogeny and

documented reports of larval schooling, this larval be-

havioral trait is likely an ancestral condition for the entire

L. latrans + L. melanonotus clade; however, additional field

observations are still needed for the majority of species in

the melanonotus species group.

The earlier evolution of egg attendance coupled with

post-hatching larval schooling would have facilitated the

evolution of more advanced behaviors such as attendance

and active defense of larvae. Parental care in the form of

attendance of eggs and larvae were reported for L. validus

(Downie, 1996), L. podicipinus (Prado et al., 2000, 2002;

Martins, 2001), L. leptodactyloides (Downie, 1996 re-

ported as “R. Cocroft and V. Morales, pers. comm.”), L. na-

talensis (Santos and Amorim, 2006), and L. pustulatus (de

Sá et al., 2007a). Only attendance of larvae was reported

in L. chaquensis (Prado et al., 2000); however, this spe-

cies also attends eggs and larvae (C. Prado and R. de Sá,

pers. obs.). Parental care in these species ranges from tad-

poles congregating closely around and/or on top of the at-

tending female (e.g., if the water close to the larval school

is disturbed) to active defense of the larvae by adults.

The most complex parental care reported includes

attendance and active defense of eggs and larvae in

Leptodactylus latrans (Fernández and Fernández, 1921;

Gallardo, 1964b; Vaz-Ferreira and Gehrau, 1974, 1975,

1986) and L. insularum (Wells and Bard, 1988; Vaira,

1997; Ponssa, 2001). Furthermore, several studies have

reported the female communicating with the larval

school. The first report was on L. latrans females where

two behaviors were observed: (1) jumping and pushing of

the larval school [“… empellón dado por la rana al grupo

muy compacto de renacuajos que los desplazo hacia la

costa…; Vaz-Ferreira and Gehrau, 1975:8] and (2) female

pelvic region maneuvers and tadpole schools following

the female [“… oscilación vertical de la zona sacroutisti-

lar y base de los miembros posteriores… este movimien-

to provoca pequeñas ondulaciones de la superficie del

agua… realiza dicho acto y es seguida de inmediato por

los renacuajos…; Vaz-Ferreira and Gehrau, 1975:8]. The

latter was subsequently described as “pumping” display

in L. insularum (Wells and Bard, 1988) and as a means

for the females to “… communicate with their tadpoles

by means of a ‘pumping’ display in which the rear part of

the body was moved up and down in the water, creating

a series of concentric waves that moved toward the tad-

poles” (Wells, 2007).

Reports of pumping maneuvers are available for

other Leptodactylus species and sometimes this behavior

is associated with observations of the female leading the

tadpoles from shallow to deeper areas of the ponds, in

some cases pushing or actively digging channels through

vegetation and soil (L. insularum: Wells and Bard, 1988,

Vaira, 1997; L. validus: Downie, 1996; L. podicipinus: Prado

et al., 2000, Martins, 2001, Prado et al., 2002, Rodrigues

et al., 2011; L. melanonotus: Hoffman, 2006; L. natalen-

sis: Santos and Amorim, 2006; L. pustulatus: de Sá et al.,

2007a; L. latrans: Rodrigues et al., 2011, L. leptodactyloi-

des: Rodrigues et al., 2011). This guiding or pushing of the

larval school in Leptodactylus (as well as other anurans)

towards deeper areas and specific microhabits within the

ponds increases tadpole survival by avoiding desiccation

or predation (particularly aquatic predators, as shown by

Rodrigues et al., 2011) and/or tapping into available food

resources or optimizing developmental temperatures

(Kok et al., 1989; Kaminsky et al., 1999; Cook et al., 2001;

de Sá et al., 2007a; Rodriguez et al., 2011).

The earliest report on the aggressive behavior of

Leptodactylus females protecting foam nests and larval

schools from approaching predators showed the female

attacking, jumping, biting, and emitting a unique call in




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L. latrans (Vaz-Ferreira and Gehrau, 1975). These authors

observed females attacking approaching predators (birds)

and reported that presentation of dead predators and

gentle introduction and movement of the observer hand

toward the foam nest triggered the same defensive be-

haviors. Aggressive behaviors toward potential predators

were also reported in L. podicipinus (Prado et al., 2002);

however, another study did not observe aggressive behav-

ior in that species (Rodrigues et al., 2011). The emission

of calls during the defensive behavior in L. latrans is likely

the same as the ‘hissing’ reported in L. insularum that may

function to frighten predators (Ponssa, 2001).

Furthermore, the extended parental attendance of

eggs and larvae is more elaborate and complex in the Lep-

todactylus latrans group + L. melanonotus group clade than

in the other species groups. Additional field observations

are needed to understand the evolution of these traits;

however, we anticipate that some, if not all, will be shown

to be ancestral for the entire L. latrans group + L. mela-

nonotus group clade. The distribution of parental care re-

ported behaviors is summarized in Fig. 6.

Larval oophagy

Among species of Leptodactylus, L. fallax is unique in

having tadpoles that lack a free-swimming larval stage and

obligatorily complete their development within the foam

nest deposited in underground chambers constructed by

the male at some distance from water sources (Brooks,

1968; Lescure, 1979; Lescure and Letellier, 1983). The

eggs are small and clutch size consists of no more than

45 eggs; hatching occur 6–10 days after oviposition, and

metamorphosis occurs in about 60 days. Both males and

females actively defend the nest and, about every 3–4

days after hatching, the female lays additional unfertil-

ized eggs that serve as the source of nutrients for the de-

veloping tadpoles (Davis et al., 2000; Gibson and Buley,

2004). Tadpoles of L. fallax become more active and move

toward the approaching female when she visits the nest to

lay unfertilized eggs (Gibson and Buley, 2004).

Recently, a second case of completion of metamor-

phosis within the nest was suggested (but not observed)

for Leptodactylus vastus (Schulze and Jansen, 2012).

Leptodactylus silvanimbus

Leptodactylus insularum

Leptodactylus bolivianus

Leptodactylus viridis


Leptodactylus chaquensis


Leptodactylus riveroi

Leptodactylus melanonotus

Leptodactylus wagneri

Leptodactylus colombiensis


Leptodactylus nesiotus

Leptodactylus pustulatus

Leptodactylus natalenis

Leptodactylus petersii

Leptodactylus leptodactyloides

Leptodactylus grisegularis

Leptodactylus discodactylus

Leptodactylus podicipinus

Leptodactylus diedrus


?

sp

Leptodactylus pentadactylus species group

Leptodactylus fuscus species group

Figure 6. Distribution of some reproductive traits reported in Leptodactylus. Optimizations are ambiguous due to extensive missing data; states marked

on internal nodes are unambiguously present in the respective hypothetical ancestors (although the state might have originated earlier) and are known

to occur in all descendant terminals (reproductive biology and larvae of L. viridis have not been documented; = ?). Yellow dot = larval schooling; green

dot = larval attendance; red dot = complex parental care. Complex parental care extends beyond attendance and includes such behaviors as active defense

against predators, communication with larvae, and guiding larvae through the pond; see text for description.




S22


These authors suggested two reproductive modes for the

species: (1) semi-aquatic oviposition (foam nest in bur-

rows or underground chambers, free-swimming larval

stage present) and (2) terrestrial oviposition (foam nest

underground without unfertilized eggs, free-swimming

larval stage absent). Additional observations and studies

are needed to fully understand the reproductive biology

of L. vastus.

In Leptodactylus labyrinthicus, from the Cerrado of

Brazil, a substantial proportion of the eggs deposited in

a foam nest apparently are not fertilized and serve as

food for developing tadpoles (da Silva et al., 2005). How-

ever, there is no evidence that females return to the nest

to provision the tadpoles (Shepard and Caldwell, 2005).

Considering, (1) the report of L. vastus as possessing ter-

restrial oviposition and absence of both unfertilized eggs

and free swimming stage (at least in some populations)

and (2) that endotrophic larvae have not been described

for any Leptodactylus species, then we should add this spe-

cies as exhibiting larval oophagy.

Larval oophagy has been reported in Leptodactylus

fallax, L. knudseni, L. labyrinthicus, L. pentadactylus, L. sav-

agei, L. troglodytes, and L. vastus. Opportunistic oophagy

on heterospecific eggs was reported in free-swimming

tadpoles of L. syphax and L. labyrinthicus (da Silva and

Giaretta, 2009), L. troglodytes (Silva and Juncá, 2006),

L. vastus (Schulze and Jansen, 2012), whereas larvae of

L. rhodomystax were reported to feed on both intra- and

interspecific eggs. It is likely that opportunistic oophagy

might also occur in other species of Leptodactylus. Con-

specific obligate oophagy evolved once in the L. pentadac-

tylus group. The larvae of L. fallax are obligatorily oopha-

gous and females lay between 10,000–25,000 unfertilized

eggs, over a two-month period, to sustain the develop-

ment of a single clutch of tadpoles (Davis et al., 2000;

Gibson and Buley, 2004; Martin et al., 2007). The larvae

of other Leptodactylus species exhibit facultative oophagy.

Species with facultative larval oophagy lay their foam nest

in burrows or cavities close to or at variable distances from

the edges of water bodies; part of the larval development

occurs within the nests but it is completed as free-swim-

ming exotrophic larvae (L. savagei, Muedeking and Heyer,

1976; L. pentadactylus, Hero and Galatti, 1990; L. knud-

seni, Hero and Galatti, 1990; L. labyrinthicus, Agostinho,

1994; Rodriguez and Duellman, 1994).

Larval oophagy in nests was reported for Leptodacty-

lus savagei (Muedeking and Heyer, 1976), L. labyrinthicus,

(Agostinho, 1994; da Silva et al., 2005) and L. pentadacty-

lus (Heyer et al., 2011). It is likely that in all of these spe-

cies the larvae feed on unfertilized eggs deposited along

with the fertilized eggs, as reported for L. labyrinthicus

(da Silva et al., 2005), as supplementary nutrition during

their development. There are no reports of the female de-

positing unfertilized eggs after initial oviposition in any

of these species. Additionally, the free-swimming larvae

of these species are known to be carnivorous and canni-

balistic (Muedeking and Heyer, 1976; Hero and Galatti,

1990; Cardoso and Sazima, 1997; Eterovick and Sazima,

2000; Heyer et al., 2011); based on our phylogeny, we

agree with the previous suggestion that larval oophagy

may have facilitated the evolution of larval carnivory in

this clade (Prado et al., 2005).

The obligate oophagous tadpole is a uniquely de-

rived condition in Leptodactylus fallax. The larvae of

L. myersi and L. peritoaktites remain unknown. Recently

L. peritoaktites was recognized as a separate species from

L. pentadactylus and L. paraensis from L. labyrinthicus

(Heyer, 2005). We anticipate that this entire subclade of

species will have facultative larval oophagy and carnivory

(although L. myersi, due to its association with rocky out-

crops, might have terrestrial development and obligate

oophagy). Whereas the construction of underground re-

productive chambers characterizes the L. fuscus species

group, larval oophagy and the invasion of rocky outcrops

are traits that overall are more common in the L. penta-

dactylus species group. Distribution of reported oophagy

in Leptodactylus is summarized in Figure 5.

ACCOUNTS FOR SPECIES OF THE GENUS

LEPTODACTYLUS FITZINGER, 1826

Leptodactylus Fitzinger, 1826:38. Type species: Rana ty-

phonia Latreille in Sonnini and Latreille an X, 1801–

1802 (= Rana fusca Schneider, 1799), by subsequent

designation of Fitzinger, 1843:31.

Cystignathus Wagler, 1830:202. Type species: Cystignathus

pachypus Wagler, 1830 (= Rana pachypus Spix, 1824)

by subsequent designation of Fitzinger, 1843:31.

The subsequent designation of Rana mystacea Spix,

1824, by Lynch, 1971:187, is in error. Synonymy

by Tschudi, 1838:78 (although using Cystignathus);

Boulenger, 1882:237.

Gnathophysa Fitzinger, 1843:31. Type species: Rana laby-

rinthica Spix, 1824, by original designation. Synon-

ymy by Jiménez de la Espada, 1875:36; Boulenger,

1882:237.

Sibilatrix Fitzinger, 1843:31. Type species: Cystignathus

gracilis Duméril and Bibron, 1841, by original desig-

nation. Synonymy by Jiménez de la Espada, 1875:44.

Plectromantis Peters, 1862:232. Type species: Plectroman-

tis wagneri Peters, 1862, by monotypy. Synonymy by

Nieden, 1923:479.

Entomoglossus Peters, 1870:647. Type species: Entomo-

glossus pustulatus Peters, 1870 by monotypy. Syn-

onymy by Boulenger, 1882:237.

Pachypus Lutz, 1930:22. Type species: None designated.

Proposed as a subgenus of Leptodactylus. Preoc-

cupied by Pachypus d’Alton, 1840 (Mammalia) and

Pachypus Cambridge, 1873 (Arachnida).




S23


Cavicola Lutz, 1930:2, 22. Type species: None designated.

Coined as a subgenus of Leptodactylus. Preoccupied

by Cavicola Ancey, 1887 (Mollusca).

Vanzolinius Heyer, 1974a:88. Type species: Leptodacty-

lus discodactylus Boulenger, 1884 “1883”, by origi-

nal designation. Synonymy by de Sá, Heyer, and

Camargo, 2005a:87–97; Frost, Grant, Faivovich,

Bain, Haas, Haddad, de Sá, Channing, Wilkinson,

Donnellan, Raxworthy, Campbell, Blotto, Moler,

Drewes, Nussbaum, Lynch, Green, and Wheeler,

2006:207.

Leptodactylus fuscus species group

Leptodactylus albilabris (Günther, 1859a)

(Plate 1A)

Cystignathus albilabris Günther, 1859a:217. Type local-

ity: West Indies, St. Thomas. Lectotype: BMNH

1947.2.1760, adult male.

Leptodactylus dominicensis Cochran, 1923:184–185. Type

locality: Dominican Republic, El Seibo Province, Las

Cañitas. Holotype: USNM 65670, adult male.

Etymology. From the Latin albi (white) and labris (lip).

Adult morphology. Moderate size, female snout–vent

length (SVL) 32.9–48.1 mm (X = 41.2 mm), male SVL

30.0–43.1 mm (X = 41.2 mm); adult male snout spatulate;

males lack thumb spines and chest spines; light lip stripe

almost always distinct (94% of specimens); dorsal folds

absent; complete pair of dorsolateral folds; lateral folds

absent or interrupted; posterior thigh with light stripe;

upper shank barred; belly uniform light to lightly mottled

or speckled; toes without lateral fringes (Heyer, 1978:37–

38; Joglar et al., 2005:74–87).

Similar species. Leptodactylus albilabris is the only spe-

cies of the genus that occurs on the following Antillean

islands: Anegada, Dominican Republic, Puerto Rico, St.

Croix, St. John, St. Thomas, and Tortola.

Larval morphology. Maximum total length (Gosner

36) 42.6 mm; oral disk anteroventral; tooth row formula

2(2)/3; tail mottled (Heyer, 1978:37–38).

Advertisement call. Dominant (= fundamental) frequen-

cy 2,000–2,800 Hz; call duration 0.046–0.050 s; each call

with 2 pulses; rising frequency modulations throughout

call; call rate 4/s; no harmonic structure (Heyer, 1978:37–

38; Joglar et al., 2005:74–87) (Fig. 7).

Distribution. Puerto Rico, Puerto Rican bank islands,

Dominican Republic (Fig. 8).

Leptodactylus bufonius Boulenger, 1894 (Plate 1B)

Leptodactylus bufonius Boulenger, 1894:348. Type lo-

cality: “Asuncion, Paraguay.” Lectotype: BMNH

1947.2.17.72, female.

Etymology. From the Latin bufo (toad), bufonius

(toad-like).

Adult morphology. Moderate size, female SVL 49.0–

61.8 mm (X = 54.7 mm), male SVL 45.5–59.4 mm

(X = 52.2 mm); adult male snout spatulate; males lack

thumb spines and chest spines; light upper lip stripe

absent; dorsal folds absent; dorsolateral folds usu-

ally absent, sometimes weak; lateral folds complete;

no light stripe on posterior thigh; upper shank barred;

belly uniform light; toes without lateral fringes (Heyer,

1978:44–46).

Similar species. Leptodactylus bufonius occurs in Argen-

tina, Bolivia, Brazil, and Paraguay. Similar species from

these countries that lack toe fringes and dorsal folds are

L. cupreus, L. elenae, L. latinasus, L. mystaceus, L. mystaci-

nus, L. troglodytes and some individuals of L. notoaktites

and L. spixi. Leptodactylus bufonius lacks a light longitu-

dinal pinstripe on the posterior thigh; L. cupreus, L. ele-

nae, L. latinasus, L. mystaceus, L. notoaktites, and L. spixi

have distinct light stripes on the posterior thigh. Lepto-

dactylus bufonius usually lack dorsolateral folds, but some

specimens have weak dorsolateral folds; L. mystacinus al-

ways have well-defined dorsolateral folds. Leptodactylus

bufonius is morphologically very similar to L. troglodytes.

Figure 7. Advertisement call of Leptodactylus albilabris (recording

USNM 324).

Figure 8. Distribution map of Leptodactylus albilabris.




S24


The post-tympanic gland is sometimes pigmented in

males of L. bufonius and not in L. troglodytes. Leptodacty-

lus troglodytes (both males and females) have a calcified

pseudo-odontoid (Sebben et al., 2007) on the mandibular

symphysis that is unique within Leptodactylus. Leptodac-

tylus troglodytes differ in advertisement calls (dominant

frequency range 1,000–2,000 Hz in L. bufonius, 2,600–

3,200 Hz in L. troglodytes) and distribution in Brazil

(L. bufonius in Mato Grosso, L. troglodytes in Bahia, Ceará,

Goiás, Minas Gerais, Paraíba, Pernambuco, Piauí, Rio

Grande do Norte, Sergipe).

Larval morphology. Total length (Gosner 37) 38.9 mm,

oral disk anteroventral, tooth row formula 2(2)/3(1), tail

weakly mottled (data from Cei, 1980).

Advertisement call. Dominant (= fundamental) fre-

quency modulated between 1,000–2,000 Hz; call duration

0.2 s; each call comprised of a single note; rising frequen-

cies throughout call; call rate 1.25 calls/s; no harmonic

structure (Heyer 1978:44–45) (Fig. 9).

Distribution. Arid habitats in Argentina, Bolivia, Brazil,

and Paraguay (Fig. 10).

Leptodactylus caatingae Heyer and Juncá, 2003

(Plate 1C)

Leptodactylus caatingae Heyer and Juncá, 2003:324. Type

locality: Brazil, Bahia, Joazeiro. Holotype: ZUEC

8833, adult male.

Etymology. Latinized from the Portuguese word caat-

inga, referring to the characteristic distribution of this

species within the Caatinga Morphoclimatic Domain

(Ab’Sáber, 1977).

Adult morphology. Small, female SVL 36.2–39.1 mm

(n = 2), male SVL 32.1–36.9 mm (X = 34.7 mm); adult

male snout spatulate; males lack thumb spines and

chest spines; light lip stripe usually distinct, smoothly

or roughly defined; dorsal folds absent; dorsolateral

folds absent or interrupted; lateral folds absent; poste-

rior thigh usually with light stripe; upper shank barred;

belly with uniform dispersion of melanophores to speck-

led; distinct white tubercles on outer surface of tarsus

and sole of foot; toes lacking fringes (Heyer and Juncá,

2003).

Similar species. Leptodactylus caatingae occurs only

in Brazil. Other species that occur in Brazil that have

a distinct light stripe on the posterior surface of the

thigh and distinct white tubercles on the outer surface

of the tarsus and sole of foot are L. elenae, L. latinasus,

and L. mystaceus. Leptodactylus elenae and L. mystaceus

have distinct, complete dorsolateral folds (indicated by

color pattern in poorly preserved specimens); L. caat-

ingae has interrupted, indistinct, or no dorsolateral

folds. Leptodactylus caatingae and L. latinasus have

considerable morphological and color pattern over-

lap and cannot be consistently diagnosed from each

other based on these features. The advertisement calls

of L. caatingae are pulsed, with dominant frequencies

ranging from 940–1,620 Hz; the calls of L. latinasus are

not pulsed and have higher dominant frequencies rang-

ing from 3,000–3,780 Hz. Leptodactylus caatingae and

L. latinasus have completely allopatric distributions

Figure 9. Advertisement call of Leptodactylus bufonius (recording USNM

19).

Figure 10. Distribution map of Leptodactylus bufonius.




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in Brazil (the southernmost state in Brazil in which

L. caatingae occurs is Espírito Santo; the northernmost

occurrence of L. latinasus is the Brazilian state of Rio

Grande do Sul).

Larval morphology. Total length (Gosner 38) 32.1 mm;

oral disk ventral; tooth row formula 2(2)/3(1); dorsal tail

musculature homogeneously brown, ventral tail muscu-

lature light cream with scattered brown spots and mark-

ings, fins translucent with scattered brown markings on

the edges (Magalhães et al., 2013:205–206).


quency 1,070–1,120 Hz; call duration 0.06–0.08 s; each

call with 7–8 distinct pulses; rapidly rising frequency

modulation throughout each call; call rate 2.6/s; no har-

monic structure (Heyer and Juncá, 2003) (Fig. 11).

Distribution. Northeast Brazil (Fig. 12).

Leptodactylus camaquara Sazima and Bokermann,

1978 (Plate 1D)

Leptodactylus camaquara Sazima and Bokermann,

1978:907. Type locality: “km 132 da Estrada Vespa-

siano a Conceição do Mato Dentro, Serra do Cipó,

[1500 m] Jaboticatubas, Minas Gerais, Brasil.” Holo-

type: MZUSP 73693 [formerly WCAB 48120], adult

male.

Etymology. The name camaquara is an indigenous term

for pond dweller in allusion to the species’ habit of mak-

ing excavations (translated from Sazima and Bokermann,

1978:908).

Adult morphology. Small size, female SVL 31.8–38.3 mm

(X = 34.8 mm), male SVL 30.7–33.7 mm (X = 32.2 mm);

males and females with weakly protruding snouts; males

lack thumb spines and chest spines; light lip stripes ir-

regular, well to poorly ill-defined; a pair of weakly devel-

oped dorsal folds; a pair of weakly developed dorsolateral

folds; lateral folds complete; posterior thighs with a series

of small light spots in the same field as the continuous

light thigh stripes occurring in other species; upper shank

barred; belly uniform light; toes without lateral fringes

(Sazima and Bokermann, 1978:907–909).

Similar species. All specimens of Leptodactylus cam-

aquara have a series of small light spots on the posteri-

or thigh where light stripes occur in many other species

of Leptodactylus. Leptodactylus cunicularius, L. jolyi, and

L. tapiti are the only other known species in which some

specimens have a series of light spots on the posterior

thigh. Leptodactylus camaquara lacks a light longitudinal

stripe on the dorsal shank surface; L. jolyi either has a

light stripe or a series of light dots on the dorsal shank

surface. Leptodactylus camaquara is morphologically simi-

lar to L. cunicularius and L. tapiti. Leptodactylus camaquara

is sympatric with L. cunicularius at the Serra do Cipó

(Minas Gerais, Brazil); L. tapiti occurs at the Chapada dos

Veadeiros (Goiás, Brazil). The advertisement calls differ

between L. camaquara (single calls of 0.3 s duration) and

L. cunicularius (calls organized in bouts of 1–2 s duration,

with each call 0.07 s duration).

Larval morphology. Total length (Gosner 39) 37 mm;

oral disk anteroventral; tooth row formula 2(2)/3(1); tail

mottled (Sazima and Bokermann, 1978:908–909).


cy 2,300–2,800 Hz; call duration 0.3 s; each call a single

pulse; rising frequency modulations throughout call; call

rate 0.75/s; calls with harmonic structure, third harmonic

not quite as intense as dominant frequency (Sazima and

Bokermann, 1978:905, 908) (Fig. 13).

Figure 11. Advertisement call of Leptodactylus caatingae (recording

USNM 22).

Figure 12. Distribution map of Leptodactylus caatingae.




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Distribution. Known only from the Serra do Cipó, Minas

Gerais, Brazil (Fig. 14).

Leptodactylus cunicularius Sazima and Bokermann,

1978 (Plate 1E)

Leptodactylus cunicularius Sazima and Bokermann, 1978.

Type locality: “km 114/115 da Estrada de Vespasia-

no a Conceição do Mato Dentro, Serra do Cipó, Jabo-

ticatubas, Minas Gerais, Brasil.” Holotype: MZUSP

73685 (formerly WCAB 48000), adult male.

Etymology. The Latin word cunicularius means miner or

burrower and alludes to excavations the frogs create that

are similar to those dug by rabbits.

Adult morphology. Small–moderate size, female SVL

43.6–44.9 mm (X = 44.2 mm), male SVL 35.5–43.2 mm

(X = 39.2 mm); adult male snout weakly spatulate; males

lack thumb spines and chest spines; light lip stripe dis-

tinct; weak pair of sinuous dorsal folds; weak pair of sinu-

ous dorsolateral folds; lateral folds interrupted; posterior

thigh with a series of light spots or a light stripe; upper

shank barred or with a series of light dots; belly uniform

light; toes without lateral fringes (Heyer et al., 2008).

Similar species. Leptodactylus cunicularius occurs in Serra

do Espinhaço and Serra da Mantiqueira (Minas Gerais, Bra-

zil) and is similar to L. camaquara, L. furnarius, and L. jolyi,

which also occur in the Serra do Cipó. The dorsolateral folds

of L. cunicularius are sinuous, not straight throughout their

length; the dorsolateral folds of L. furnarius and L. jolyi are

slightly curved just behind the tympanum and straight on

the rest of the body. Leptodactylus cunicularius is very simi-

lar to L. camaquara morphologically. Some individuals of

L. cunicularius have a series of light dots where the light

posterior thigh stripes occur in other species, whereas all

individuals of L. camaquara have a series of light dots on

Figure 13. Advertisement call of Leptodactylus camaquara (recording

USNM 328).

Figure 14. Distribution map of Leptodactylus camaquara.

Figure 15. Advertisement call of Leptodactylus cunicularius (recording

USNM 242).

Figure 16. Distribution map of Leptodactylus cunicularius.




S27


the posterior thighs. Some individuals of L. cunicularius

have a series of light dots on the upper shank; no individu-

als of L. camaquara have a series of light dots on the up-

per shank. The advertisement calls of L. cunicularius and

L. camaquara are very different. Leptodactylus cunicularius

produce individual notes at a rate of 12 per second and

the duration of each note is about 0.07 s; individual notes

of L. camaquara occur at a rate of less than 1 per second

(0.75/s) and each note duration is about 0.3 s.


38) 39.0 mm; oral disk anteroventral; tooth row for-

mula 2(2)/3(1); tail mottled (Sazima and Bokermann,

1978:905–906).


cy 2,200–2,700 Hz; call duration 1–2 s with 2–4 s inter-

vals between calls; each call consisting of a single-pulsed

note; each note with rising frequency modulations; call

= note = pulse rate 3.1/s; call with harmonic structure

(Sazima and Bokermann, 1978:905–906) (Fig. 15).

Distribution. Known only from the Serra do Espinhaço

and Serra da Mantiqueira, Minas Gerais, Brazil (Fig. 16).

Leptodactylus cupreus Caramaschi, Feio, and São

Pedro, 2008 (Plate 1F)

Leptodactylus cupreus Caramaschi, Feio, and São Pedro,

2008:44. Type locality: Lagoa das Bromélias (20°25’S,

43°29~ , 1,227 m above sea level), Parque Estadual

da Serra do Brigadeiro, District of Careço, Municipal-

ity of Ervália, State of Minas Gerais, Southeastern

Brazil. Holotype: MNRJ 47752, adult male.

Etymology. The Latin adjective cupreus refers to the cop-

per coloration of the species.


57.9 mm (X = 56.8 mm), male SVL 50.1–57.0 mm


thumb spines and chest spines; light lip stripe distinct; no

dorsal folds; dorsolateral folds thick, from anterior third

of body to groin, marked by a lighter coloration than that

of flanks and dorsum; lateral folds absent; flanks from

bright copper with scattered small markings to solid dark;

posterior thigh with light stripe; upper shank indistinctly

barred; belly whitish grey with scattered irregular cream

markings; toes without lateral fringes (Caramaschi et al.,

2008:44–54; Cassini et al., 2013).

Similar species. Leptodactylus cupreus is a member of the

L. mystaceus complex comprising L. didymus, L. elenae,

L. mystaceus, L. notoaktites, and L. spixi that is defined by

having two distinct dorsolateral folds (no dorsal or lateral

folds), a distinct light upper lip stripe, a distinct longitudi-

nal light stripe on the posterior surface of the thighs and

the sole of the foot with prominent white tubercles. Lepto-

dactylus cupreus lacks dark markings/spots on the dorsum,

the dorsal surfaces of the thighs and shanks are not dis-

tinctly barred, and posses a divided outer metacarpal tu-

bercle; all other members of the L. mystaceus complex have

distinct dorsal patterns of dark marks, the dorsal surfaces

of thighs and shanks are distinctly barred, and have entire

outer metacarpal tubercles. In addition, the presence of

small spines on the dorsal surface of the tibia of L. cupreus

distinguished it from L. mystaceus (spines on tibia absent).



2(2)/3(1); tail mottled (Motta et al., 2010:65–68).


cy 2,800–3,058 Hz; call groups given irregularly in long

Figure 17. Advertisement call of Leptodactylus cupreus.

Figure 18. Distribution map of Leptodactylus cupreus.




S28


and fast sequence of notes, note duration 0.16/s; notes

not pulsed; rising frequency modulations through most

of note with a terminal drop in frequency; note rate about

12/s; two distinct harmonics in addition to fundamental

(Caramaschi et al., 2008:50) (Fig. 17).

Distribution. Known from the Brazilian states of Bahía,

Espirito Santo, and Minas Gerais (Fig. 18).

Leptodactylus didymus Heyer, García-Lopez, and

Cardoso, 1996 (Plate 2A)

Leptodactylus didymus Heyer, García-Lopez, and Cardoso,

1996:25. Type locality: Peru: Madre de Dios; Tam-

bopata Reserved Zone, 12°50’S, 69°17~ . Holotype:

USNM 332861, adult male.

Etymology. From the Greek didymus, double or twin, re-

ferring to the morphological similarity between Leptodac-

tylus didymus and L. mystaceus.


53.5 mm (X = 49.2 mm), male SVL 45.9–52.2 mm

(X = 49.0 mm); adult male snout weakly spatulate; males

lacking thumb spines and chest spines; muted light upper

lip stripe; dorsal folds absent; distinct pair of dorsolateral

folds; lateral folds interrupted or absent; posterior thigh

with light stripe; upper shank barred; belly uniform light;

toes without lateral fringes (Heyer et al., 1996a).

Similar species. Leptodactylus didymus is known from the

Bolivian departments of Beni, La Paz, Pando, the Brazil-

ian states of Acre, Amazonas, and the Peruvian depart-

ment of Madre de Dios. The other similar species occur-

ring within the distribution of L. didymus are L. fuscus and

L. mystaceus. Leptodactylus fuscus have a pair of longitudi-

nal dorsal folds; L. didymus lack dorsal folds. There are no

morphological features that distinguish L. didymus from

L. mystaceus. The advertisement call of L. didymus exhib-

its a single or two partial pulses; the call of L. mystaceus

has 9–17 pulses.

Larval morphology. Unknown.


quency 510–1,510 Hz; call duration 0.09–0.32 s; each

call consists of a single pulse or two partial pulses; rising

frequency modulation through entire call or with a brief

terminal drop in frequency; call rate 1.4–3.1/s; harmonic

structure present (Heyer et al., 1996a, Köhler and Löt-

ters, 2002) (Fig. 19).

Distribution. Bolivian departments of Beni, La Paz, Pan-

do; Brazilian states of Acre, Amazonas; Peruvian depart-

ment of Madre de Dios (Fig. 20).

Leptodactylus elenae Heyer, 1978 (Plate 2B)

Leptodactylus elenae Heyer, 1978:45. Type locality: Argen-

tina, Salta, Embarcación. Holotype: LACM 92096,

adult female.

Etymology. Named for W.R. and M.H. Heyer’s daughter,

Elena.


48.6 mm (X = 43.8 mm), male SVL 37.9–46.4 mm

(X = 43.2 mm); adult male and female snouts not spat-

ulate nor protruding beyond the lower jaw; males lack

thumb spines and chest spines; light upper lip stripe usu-

ally (77% of specimens) distinct; dorsal folds absent; dis-

tinct pair of dorsolateral folds; lateral folds absent, inter-

rupted, or present; posterior thigh with light stripe; upper

shank barred; ventral surface of belly mostly uniformly

light with few melanophores or clumps of melanophores

Figure 19. Advertisement call of Leptodactylus didymus (recording

USNM 205).

Figure 20. Distribution map of Leptodactylus didymus.




S29


on lateral-most areas of the belly; toes without lateral

fringes; posterior surfaces of the shank and sole of foot

with distinct white tubercles (Heyer, 1978:45–46, Heyer

and Heyer, 2002:1–5).

Similar species. Leptodactylus elenae occurs in arid re-

gions of northwest Argentina (Jujuy, Salta), Brazil (Mato

Grosso, Mato Grosso do Sul), Bolivia (Beni, La Paz, Santa

Cruz), and Paraguay. Similar species that occur with L. ele-

nae are L. bufonius, L. fuscus, L. latinasus, and L. mystaci-

nus. Leptodactylus bufonius and L. mystacinus lack a light

stripe on the posterior thigh, L. elenae have a light thigh

stripe. Leptodactylus elenae lack dorsal folds whereas

L. fuscus have a pair of dorsal folds. Leptodactylus elenae

are larger than L. latinasus (female SVL 29.1–35.7 mm,

male SVL 27.0–37.9 mm) and dorsolateral folds are ab-

sent or indistinct in L. latinasus.



2(2)/3(1); tail mottled (Prado and d’Heursel, 2006, Vera

Candioti et al., 2007).


quency 700–870 Hz at beginning of call, 1,370–1,500 Hz

at end of call; each call a single note, unpulsed or weak-

ly pulsed in mid-call; rising frequency modulations

throughout call; call rate 64–120/min; harmonics either

absent or present (Barrio, 1965, Heyer and Heyer, 2002)

(Fig. 21).

Distribution. Arid regions of Argentina (Jujuy, Salta),

Brazil (Mato Grosso, Mato Grosso do Sul), Bolivia (Beni,

La Paz, Santa Cruz), and Paraguay (Fig. 22).

Leptodactylus fragilis (Brocchi, 1877) (Plate 2C)

Cystignathus fragilis Brocchi, 1877:182. Type locality: “Cet

animal a été envoyé de Tehuantepec [Mexique].” Ho-

lotype: MNHN 6316, female.

Leptodactylus fragilis: Brocchi, 1881–1883:19. First usage

of fragilis with the genus Leptodactylus.

Leptodactylus mystaceus labialis: Shreve, 1957:246.

Etymology. The Latin fragilis means brittle. It is unclear

why Brocchi used this name.


(X = 36.3 m), male SVL 27.0–43.0 mm (X = 34.8 mm);

adult male snout spatulate; males without thumb spines

and chest spines; indistinct light upper lip stripe (97% of

specimens); dorsal folds absent; weak dorsolateral folds;

lateral folds interrupted or absent; posterior thigh with

light stripe; upper shank barred; belly without pattern or

with small spots on lateral and anterior portions of belly;

toes without lateral fringes (Heyer et al., 2006).

Similar species. Leptodactylus fragilis has been misiden-

tified in the literature as L. melanonotus. Leptodactylus

fragilis lacks toe fringes; L. melanonotus has toe fringes.

Otherwise, L. fragilis is similar to L. fuscus and L. poecilo-

chilus with which it co-occurs. Leptodactylus fuscus has a

pair of dorsal folds; L. fragilis lacks dorsal folds. Leptodac-

tylus poecilochilus has distinct dorsolateral folds and al-

most always (93% of specimens) lacks white tubercles on

the sole of the foot; L. fragilis has indistinct dorsolateral

Figure 21. Advertisement call of Leptodactylus elenae (recording USNM

180).

Figure 22. Distribution map of Leptodactylus elenae.




S30


folds and has many white tubercles on the sole of the

foot.

Larval morphology. Maximum total length (Gosner 32–

34) 32 mm; oral disk anteroventral; tooth row formula

2(2)/3(1); tail mottled (Heyer et al., 2006).


quency 600–2,010 Hz; call duration ranges from 0.11–

0.20 s; call consists of one or two notes and may be par-

tially or fully pulsed; call frequency modulated, rising

throughout call, sometimes a short drop in frequency

at the beginning or end of call; call rate 1.5–150 calls/

min; call with harmonic structure (Heyer et al., 2006:2)

(Fig. 23).

Distribution. From southernmost Texas (USA) on the

Atlantic coast and Colima, Mexico on the Pacific coast

through Middle America to northern Colombia includ-

ing the Cauca and Magdalena valleys, the Río Arauca

and Río Apure drainages in Colombia and northern Ven-

ezuela extending as far as the Venezuelan State of Sucre

(Fig. 24).

Leptodactylus furnarius Sazima and Bokermann,

1978 (Plate 2D)

Leptodactylus furnarius Sazima and Bokermann, 1978:899.

Type locality: “Campo Grande, [900 m] Paranapiaca-

ba, São Paulo, Brasil.” Holotype: MZUSP 73678 [for-

merly WCAB 47949], adult male.

Leptodactylus laurae Heyer, 1978:59. Type locality: Brazil:

Minas Gerais; Água Limpa, Juiz de Fora. Holotype:

MZUSP 130, adult male. Placed in synonymy of

L. furnarius by Heyer, 1983:271.

Etymology. Sazima and Bokermann (1978:901) indicat-

ed that the Latin furnarius was equivalent to the Portu-

guese word “oleiro” = potter, maker of earthenware ves-

sels. (Jaeger, 1955:106, translates furnarius as baker.) The

name is in allusion to the species’ construction of incubat-

ing chambers, similar to earthen ovens.


36.0–49.6 mm SVL (X = 42.5 mm SVL), male SVL 30.7–

46.4 mm SVL (X = 36.6 mm SVL); adult male snout round-

ed (usually) or weakly spatulate; males lack thumb spines

and chest spines; light upper lip stripe present, usually

(71% of specimens) distinct or indistinct (29% of speci-

mens); one pair of dorsal folds; one pair of dorsolateral

folds; lateral folds complete; posterior thigh with distinct

(51% of specimens) or indistinct (49% of specimens) light

stripes; upper shanks barred; belly uniform light; toes

without lateral fringes (Heyer and Heyer, 2004).

Similar species. Leptodactylus furnarius occurs through-

out the semi-arid Cerrado and Campo Rupestre morpho-

climatic domains and marginally occurs in the Atlantic

Forest morphoclimatic domain. Other similar species oc-

curring with L. furnarius are L. elenae, L. fuscus, L. graci-

lis, L. latinasus, L. mystaceus, L. mystacinus, L. notoaktites,

and L. plaumanni. Leptodactylus gracilis and L. plaumanni

have thin, light longitudinal stripes on the upper shanks;

L. furnarius lacks light stripes on the upper surface of the

shanks. Leptodactylus elenae, L. latinasus, L. mystaceus,

L. mystacinus, and L. notoaktites lack a pair of dorsal folds;

L. furnarius have a pair of dorsal folds. Leptodactylus fur-

narius have a light mid-dorsal stripe; most individuals

(90%) of L. fuscus lack light mid-dorsal stripes. The legs

of L. furnarius are longer than those of L. fuscus (e.g., fe-

male L. furnarius shank/SVL ratios range from 54–63%

and males range from 53–66% whereas female L. fuscus

shank/SVL ratios range from 43–52% and males range

from 40–51%).

Larval morphology. Maximum total length (Gos-

ner 38) 41 mm; oral disk anteroventral; tooth row for-

mula 2(2)/3(1); tail mottled (Sazima and Bokermann,

1978:901, 909).

Figure 23. Advertisement call of Leptodactylus fragilis (recording USNM

225).

Figure 24. Distribution map of Leptodactylus fragilis.




S31



cy 2,600–3,400 Hz; call duration 0.04 s; each call = note

with 3–4 pulses; rising frequency modulation throughout

call; call rate ca. 200/min to 450/min; no evident har-

monic structure (Sazima and Bokermann, 1978:901, 903;

Heyer and Heyer, 2004:1) (Fig. 25).

Distribution. Primarily arid habitats in the Brazilian

states of Distrito Federal, Goiás, Mato Grosso, Minas

Gerais, Paraná, Rio Grande do Sul, São Paulo, and north-

eastern Uruguay (Fig. 26).

Leptodactylus fuscus (Schneider, 1799) (Plate 2E)

Rana virginica Laurenti, 1768:31. Type locality: Not des-

ignated. Holotype: Frog illustrated by Seba, 1734,

plate 75, fig. 4 by original designation. Considered

(as Rana virginica Merrem, 1820, a subsequent us-

age) a synonym of Cystignathus fuscus by Günther,

1859b “1858”:28, and (under Cystignathus typhoni-

us) by Duméril and Bibron, 1841:402. Junior hom-

onym of Rana virginica Laurenti, 1768.

Rana fusca Schneider, 1799:130. Type locality: Implied to

be from Surinam. Syntypes: “Museo Lev. Vincentii,”

“Museo Lampiano,” presumed lost. MNHN 680, a

male, designated Neotype by Heyer, 1968:160–162.

Lynch, 1971:186–187 cited W.C.A. Bokermann

[pers. comm.] that some of the original syntypes

were still extant and without study of these, Heyer’s

neotype designation should not be accepted. Syn-

types of Rana fusca Schneider have not been located.

Rana typhonia Daudin an XI 1802 or 1803:55–56. Type

locality: “Amérique meridionale” given as Surinam

by Heyer, 1978:50. Syntypes: MNHN 680 (2 speci-

mens) according to Guibé, 1950 “1948”:30. MNHN

680 designated lectotype (and neotype of Rana fusca

Schneider, 1799) by Heyer, 1968:160–162. Syn-

onymy by Duméril and Bibron, 1841:402; Heyer,

1968:160–162.

Rana sibilatrix Wied-Neuwied, 1824a: Heft 8: plate 47, fig-

ure 2. Also published by Wied-Neuwied, 1824b:671.

Type locality: “Ostkuste von Brasiliens … Peruhype

bei Villa Viçosa vor, am Mucuri, Caravellas …,” Bra-

zil. Restricted to “Villa Viçosa am Peruhype,” Brazil

by Müller, 1927:281. Types: Include animal figured

on plate 47, figure 2 of the original; specimens oth-

erwise not designated or located according to Heyer,

1978:30. Synonymy [and expressed doubt about re-

stricted type locality] by Heyer, 1978:30. Synonymy

with Rana typhonia Daudin by Reinhardt and Lüt-

ken, 1862 “1861”:164 and Steindachner 1867:24.

Rana pachypus var. 2 Spix, 1824:26. Type locality: “aquis

Parae” Brazil. Type(s): Not specifically stated, but

including animals figured on pl. 2, figs. 1–2 in

the original publication, formerly including ZSM

2503/0, now lost according to Hoogmoed and Gr-

uber, 1983:356. Synonymy by Peters, 1872:199;

Hoogmoed and Gruber, 1983:356.

Leptodactylus typhonia: Fitzinger, 1826:64.

Leptodactylus sibilatrix: Fitzinger, 1826:64.

Cystignathus typhonius: Wagler, 1830:203.

Cystignathus sibilatrix: Wagler, 1830:203.

Cystignathus schomburgkii Troschel, 1848:659. Type lo-

cality: “Britisch-Guiana.” Types: Not designated

and presumed lost, according to Heyer, 1978:30.

Synonym of Leptodactylus typhonius by Boulenger,

1882:240; tentative synonymy by Heyer, 1978:30.

Figure 25. Advertisement call of Leptodactylus furnarius (recording

AJC33).

Figure 26. Distribution map of Leptodactylus furnarius.




S32


Cystignathus fuscus: Günther, 1859b “1858”:28.

Leptodactylus typhonius: Boulenger, 1882:240.

Leptodactylus raniformis Werner, 1899:479. Type locality:

“Rio Meta, Llanos [Orocué],” Rio Meta, Colombia.

Holotype: Originally ZIUG, now ZFMK 28484, male,

according to Böhme and Bischoff, 1984:177. Synon-

ymy by Heyer, 1978:29.

Leptodacytlus sibilator: Müller, 1927:281. Incorrect subse-

quent spelling.

Leptodactylus sybilatrix: Cei, 1950:408. Incorrect subse-

quent spelling.

Leptodactylus sybilator: Cei, 1956:48. Incorrect subse-

quent spelling.

Leptodactylus gualambensis Gallardo, 1964a:46. Type lo-

cality: “Argentina, Salta, Urundel, 43 km al Oeste

de Orán, Río Santa María.” Holotype: MACN 9752,

adult male. Synonymy by Heyer, 1968:160–162.

Leptodactylus fuscus: Heyer, 1968:160–162.

Etymology. The Latin word fuscus translates to brown,

dark, dusky in English.


36.5–56.3 mm (X = 44.8 mm), male SVL 32.4–55.3 mm

(X = 43.4 mm); adult male snout spatulate; adult males

lacking thumb spines and chest spines; light upper lip

stripe usually distinct (81% of specimens); a pair of well-

developed dorsal folds; a pair of well-developed dorso-

lateral folds; lateral folds complete; posterior thigh light

stripe distinct; upper shank barred; belly patternless,

rarely (< 10% of specimens) with small speckles over en-

tire belly; toes lacking fringes (Heyer, 1978:50–52).

Similar species. Leptodactylus fuscus has a broad distri-

butional range from Panamá, throughout the lowlands

of South America east of the Andes to about 30° S lati-

tude. Leptodactylus fuscus and the following species have

a pair of dorsal folds and lack toe fringe: L. camaquara

(some individuals lack dorsal folds), L. cunicularius,

L. furnarius, L. gracilis, L. jolyi, L. longirostris, L. maram-

baiae, L. notoaktites, L. plaumanni, L. poecilochilus (some

individuals lack dorsal folds), L. spixi, and L. tapiti. Of

the preceding, only L. fuscus individuals usually lack a

light mid-dorsal stripe. The upper shank of L. fuscus is

barred and lacks light longitudinal stripes; all individu-

als of L. gracilis, L. marambaiae, and L. plaumanni have

a light longitudinal stripe on the upper shank; L. jolyi

has either a light stripe or a series of light dots on the

upper shank. Leptodactylus fuscus rarely have distinct

white tubercles on the sole of the foot and posterior

surface of the tarsus, but small light spots are present

on these surfaces indicating the presence of weakly de-

veloped tubercles. The posterior surface of the tarsus

and sole of the foot are smooth and uniform in color-

ation in L. furnarius, L. longirostris, and L. poecilochilus.

The posterior surface of the tarsus and sole of the foot

of L. spixi have distinct white tubercles. Leptodactylus

notoaktites has a smooth posterior surface of the tarsus.

Camargo et al. (2006) suggested that L. fuscus consists

of three species consisting of three cryptic evolutionary

lineages.



2(2)/3(1); tail mottled (Lescure, 1972:96–99; Sazima,

1975:34–35).

Figure 27. Advertisement call of Leptodactylus fuscus (recording USNM

19).

Figure 28. Distribution map of Leptodactylus fuscus.




S33



quency 1,000–2,800 Hz; call = note duration 0.16–0.17 s;

notes pulsed or partially pulsed; rising frequency modu-

lations throughout call; call rate 1/s; harmonic structure

present or absent (Heyer, 1978:18–19, 50; Marquez et al.,

1995:316) (Fig. 27).

Distribution. Lowland regions of Panamá and west

of the Andes in South America with a southern limit of

about 30° S latitude (Fig. 28).

Leptodactylus gracilis (Duméril and Bibron, 1840)

(Plate 2F)

Cystignathus gracilis Duméril and Bibron, 1840: Pl. 13,

figs. 5–7; 1841:406. Type locality: Not stated. Type:

Guibé, 1950 “1948”:30 indicating that MNHN

4490 was the holotype. de Sá, Dubois, and Ohler,

2007b:177 designated MNHN 4490 from Montevi-

deo, Uruguay, as the Neotype of C. gracilis Duméril

and Bibron, 1840.

Leptodactylus gracilis: Jiménez de la Espada, 1875:44.

Leptodactylus gracilis delattini Müller, 1968:48. Type local-

ity: Brazil, Santa Catarina, Ilha Campeche. Holotype:

MZUSP 56589, formerly SMF 4080.

Etymology. From the Latin gracilis, slender, thin.

Adult morphology. Small-moderate size, female SVL

37.2–55.3 mm (X = 44.0 mm), male SVL 31.0–52.7 mm

(X = 42.9 mm); adult male snout calloused, not spatulate;

males lack thumb spines and chest spines; light upper lip

stripe almost always distinct (95% of specimens); distinct

pair of dorsal folds; distinct pair of dorsolateral folds; lat-

eral folds interrupted or complete; light posterior thigh

stripe usually distinct (72% of specimens); upper shank

barred with a narrow, longitudinal light stripe; belly usu-

ally uniform light, sometimes small spots encroaching on

belly; toes without lateral fringes (Heyer, 1978:53–56).

Similar species. Leptodactylus gracilis occurs in Argenti-

na, Bolivia, Brazil, Paraguay, and Uruguay. Leptodactylus

fuscus and L. notoaktites also occur within the range of

L. gracilis and these taxa do not have a narrow light lon-

gitudinal stripe on the upper shank. While Leptodactylus

plaumanni is within the geographical range of L. gracilis,

there are no consistent morphological features that differ-

entiate the two. Leptodactylus gracilis occurs in Argentina,

Bolivia, Brazil, Paraguay, and Uruguay. Leptodactylus jolyi,

L. marambaiae, L. plaumanni, and L. sertanejo also occur

within the range of L. gracilis and all of these taxa have

narrow light longitudinal stripes (on narrow longitudinal

folds) on the upper shanks (some individuals of L. jolyi

have a series of light dots on the longitudinal shank folds).

Leptodactylus marambaiae only occurs on the island of

Marambaia in the State of Rio de Janeiro; L. gracilis does

not occur on Marambaia. There are no consistent morpho-

logical features that differentiate L. gracilis from L. jolyi,

L. plaumanni, and L. sertanejo. The advertisement call rate

of L. gracilis is 3–4 calls per second; that of L. jolyi is 0.1–

0.3 calls per second; that of L. plaumanni is 13–25 calls per

second; that of L. sertanejo is 0.02–0.3 calls per second.

Larval morphology. Maximum total length (ca. Gosner


2(1)/3(1); tail mottled (Langone and de Sá, 2005:50–54).

Figure 29. Advertisement call of Leptodactylus gracilis (recording USNM

11).

Figure 30. Distribution map of Leptodactylus gracilis.




S34



quency 500–2,400 Hz; call = partially pulsed note dura-

tion 0.04–0.05 s; call pulsed or partially pulsed; rising fre-

quency modulations throughout call; note rate about 4/s;

harmonic structure present or absent (Heyer, 1978:54–

56) (Fig. 29).

Distribution. Argentina, Bolivia, Brazil, Paraguay, and

Uruguay (Fig. 30).

Comment. De Sá et al. (2007c:175–178) observed that

Cystignathus gracilis Duméril and Bibron, 1840 was based

on three figures showing a single specimen and bearing

the name. However, no particular individual was identi-

fied as the source of the figures and no locality data was

provided with the original illustration. Duméril and Bi-

bron (1841:406–407) briefly described this species and

stated that the description was based on several specimens

(number not given) collected by d’Orbigny in Montevideo;

however, no specimen was identified as the illustrated ho-

lotype. De Sá et al. (2007c) noted that Guibé designated

the holotype without justification although several speci-

mens comprise the type series and no extant specimen can

be undoubtedly identified as the holotype. Consequently,

de Sá et al. (2007c) designated and described adult male

MNHN 4490 from Montevideo, Uruguay, as the neotype

of C. gracilis Duméril and Bibron 1840.

The subspecies Leptodactylus gracilis delattini was

rejected by Heyer (1978:36) and García-Pérez and Heyer

(1993:51); and subsequently resurrected by Silva et al.,

(2004:185–196), stating “… differences in the vocaliza-

tion are subtle, but they are distinguished by some mor-

phological traits and reproductive patterns. Leptodactylus

gracilis delattini is geographically isolated; it is confined to

a coastal island in the State of Santa Catarina, and has

a specific identity, distinct from that of L. gracilis graci-

lis that has a wider distribution. Analysis based on cyto-

chrome b sequence indicated that L. gracilis gracilis and

L. gracilis delattini do not have any divergence, so that

they should remain as valid subspecies.”

Leptodactylus jolyi Sazima and Bokermann, 1978

(Plate 3A)

Leptodactylus jolyi Sazima and Bokermann, 1978:902.

Type locality: Brazil, São Paulo, Paranapiacaba, Cam-

po Grande, 900 m. Holotype: MZUSP 73726 (for-

merly WCAB 47969), adult male.

Etymology. Named for Professor Aylthon B. Joly, who

enthusiastically dedicated the last years of his life to bo-

tanical and zoological exploration in the Serra do Cipó.

Adult morphology. Data lacking for females. Moderate

size, male SVL 43.3–48.6 mm (X = 46.3 mm); adult male

snout weakly spatulate; males lacking thumb spines and

chest spines; light upper lip stripe usually faint; dorsal,

dorsolateral, and lateral folds well developed; posterior

thigh with a light stripe or a series of light spots; upper

shank barred with a thin longitudinal light stripe or a se-

ries of light dots; belly uniform light; toes without lateral

fringes (Sazima and Bokermann, 1978:902–904; Giaretta

and Costa, 2007:1–10).

Similar species. Leptodactylus jolyi was restricted to

the vicinity of Paranapiacaba, State of São Paulo, Brazil

(fide Giaretta and Costa, 2007); however, it has a more

extensive distribution. In the Paranapiacaba region, only

L. gracilis shares with L. jolyi thin and light longitudinal

stripes on the upper shanks. A dark supratympanic stripe

extends only above the tympanum in L. jolyi; in L. gracilis

the supratympanic stripe extends from above the tym-

panum and continues posterolaterally behind the tym-

panum. The vomerine teeth of L. jolyi were reported to

Figure 31. Advertisement call of Leptodactylus jolyi (recording USNM

238).

Figure 32. Distribution map of Leptodactylus jolyi.




S35


be in two straight series, whereas those of L. gracilis are

distinctly arched (Giaretta and Costa, 2007). The call rate

of L. jolyi is 0.1–0.3/s, and that of L. gracilis is 2.5–4.0/s

(Sazima and Bokermann, 1978:902–904; Giaretta and

Costa, 2007:1–10).


state 38) 45.0 mm; oral disk anteroventral; tooth row

formula 2(2)/3(1); tail mottled (Sazima and Bokermann,

1978:903, 909).


quency 900–2,600 Hz (Sazima and Bokermann, 1978),

1,500–2,500 Hz (Giaretta and Costa, 2007); call duration

0.03–0.04 s; 1–3 pulses/call; rising frequency modulation

throughout call; call rate 24/min; with or without har-

monic structure (Sazima and Bokermann, 1978:903–904;

Giaretta and Costa, 2007:3, 6) (Fig. 31).

Distribution. Paranapiacaba region, State of São Paulo,

Brazil and in open areas of the Atlantic forest and in the

Cerrados of eastern Brazil (Fig. 32).

Leptodactylus labrosus Jiménez de la Espada, 1875

(Plate 3B)

Leptodactylus labrosus Jiménez de la Espada, 1875:36.

Type locality: Orillas del Río Daule, Pimocha,

[Guayas], Ecuador. Lectotype: MNCN 3524, female.

Leptodactylus curtus Barbour and Noble, 1920:405. Type

locality: Bellavista, Cajamarca, Peru. Holotype: MCZ

5281, juvenile female.

Etymology. The Latin labrosus translates as thick-lipped.


71.2 mm (X = 59.2 mm), male SVL 47.6–67.4 mm

(X = 56.5 mm); males and females with spatulate snouts;

males lack thumb spines and chest spines; light upper lip

stripe indistinct or absent; dorsal folds absent; dorsolat-

eral folds indistinct or absent; lateral folds interrupted or

absent; posterior thigh light stripe almost always absent

(94% of specimens) or indistinct (6% of specimens); up-

per shank barred; belly uniform light to small melano-

phore blotches scattered across the anterior belly and ex-

tending centrally; toes without lateral fringes, may have

vestigial basal ridges and basal web between toes 1, 2, 3

(Heyer, 1978:56–57).

Similar species. Leptodactylus labrosus occurs west of the

Andes from the Ecuadorian Province of Manabi south

to the Peruvian Departments of Cajamarca, Libertad,

and Ancash. University of Kansas specimens identified

as L. labrosus from the Department of Cuzco, Peru, were

probably misidentified; unfortunately, the specimens

were destroyed. Leptodactylus ventrimaculatus is the only

other species that occurs together with L. labrosus in Ec-

uador. The sole of the foot is usually (91% of specimens)

smooth, without tubercles, in L. labrosus; the sole of the

foot in L. ventrimaculatus has distinct, scattered or very

few, white tubercles.

Larval morphology. Chondrocranial morphology was

described by Larson and de Sá (1998) based on USNM

520294–95; the external morphology has not been

reported.

Advertisement call. The call consists of a single note with

slight frequency modulation; call duration is 64–133 ms;

118–135 calls/minute; the dominant (= fundamental) fre-

quency is 358–726 Hz (de Carvalho and Ron, 2011).

Distribution. Lowlands west of the Andes in Ecuador

and Peru (Fig. 33).

Leptodactylus laticeps Boulenger, 1918 (Plate 3C)

Leptodactylus laticeps Boulenger, 1918:431. Type locality:

“Santa Fé, Argentina.” Holotype: BMNH 98.11.24.7,

female.

Leptodactylus (Pachypus) laticeps: Vellard, 1947:464.

Etymology. The Latin roots latus (lata, latum) and ceps

refer to a broad head.

Adult morphology. Large size, female SVL 88.0–

117.0 mm (X = 105.1 mm), male SVL 94.2–109.7 mm

(X = 101.3 mm); adult male snout not spatulate; adult

males with two black spines on each thumb; adult males

Figure 33. Distribution map of Leptodactylus labrosus.




S36


with a pair of black chest spines; light upper lip stripe

absent; no dorsal, dorsolateral, or lateral folds; posterior

thigh lacking a light longitudinal stripe; upper shank with

broad dark bands; belly light to having small spots on an-

terior and lateral portions of belly; toes without lateral

fringes (Cei, 1980:355–357).

Similar species. Leptodactylus laticeps is among the most

distinctive and colorful species in the genus Leptodac-

tylus. The species has dorsal body and limb patterns of

black squares and rectangles enclosing red markings on

an overall yellow background. In preservative, the black

squares and rectangles have white areas within and are

separated by white areas. Most Leptodactylus syphax have

a more glandular dorsum with muted tile-like dorsal pat-

tern of darker and lighter browns, but no L. syphax have

white (in preservative) marks separating the dorsal “tiles.”



quency 844–1,033 Hz; call = note duration 0.18–0.21 s;

calls pulsatile; rising frequency modulations throughout

call; call rate 45–48 calls/min; at least a second harmonic

(Heyer and Scott, 2006:190–191) (Fig. 34).

Distribution. Gran Chaco of Argentina, Bolivia, and Par-

aguay (Fig. 35).

Leptodactylus latinasus Jiménez de la Espada, 1875

(Plate 3D)

Leptodactylus latinasus Jiménez de la Espada, 1875:40.

Type locality: Montevideo, Uruguay. Holotype:

MNCN 1695, adult female.

Leptodactylus prognathus Boulenger, 1888:187. Type lo-

cality: Rio Grande do Sul, Brazil; restricted to “Rio

Grande do Sul, provávelmente São Lourenção do

Sul” by Bokermann, 1966:74; restricted to “Cam-

aquã, Estado de Rio Grande do Sul, Brasil” by Klap-

penbach and Langone, 1992:189. Holotype: BMNH

1947.2.17.52, juvenile male. Synonymy by Heyer,

1969c:3.

Leptodactylus anceps Gallardo, 1964c:100. (Type locality –:

“Argentina, prov. de Tucumán, Tucumán.” Holotype

–: MACN 531, adult male.) Synonymy by Barrio,

1965:408 (as Leptodactylus prognathus). Synonymy

by Heyer, 1978:34.

Leptodactylus latinasus latinasus: Cei, 1980:325.

Leptodactylus latinasus anceps: Cei, 1980:325. Subspecies

rejected by Ponssa and Lavilla, 1998:57–63.

Etymology. The Latin adjective latus (lata, latum), mean-

ing wide, broad, and the noun nasus (nasi) meaning snout

or nose, indicate that the species has a broad snout.



adult male snout spatulate; males lacking thumb spines

and chest spines; light upper lip strip indistinct; dorsal

folds absent; dorsolateral folds indistinct to absent; lat-

eral folds interrupted to absent; posterior thigh with a

light stripe; upper shank barred; belly usually uniform

light (90% of specimens), rarely lightly mottled laterally

(10%); toes without lateral fringes (Heyer, 1978:57–59;

Heyer and Juncá, 2003).

Figure 34. Advertisement call of Leptodactylus laticeps (recording

USNM 327).

Figure 35. Distribution map of Leptodactylus laticeps.




S37


Similar species. Leptodactylus latinasus is morphologi-

cally very similar to L. fragilis, but their distributions are

distinct with L. latinasus occurring in Argentina, Brazil,

Paraguay, and Uruguay, and L. fragilis occurring from

southernmost Texas, USA through Mexico to Panamá and

Caribbean drainages of Colombia and Venezuela. In South

America, L. latinasus occurs in sympatry with a single spe-

cies that lacks toe fringes and has distinct white tubercles

on the posterior surfaces of the shank and sole of foot—

L. elenae. The dorsolateral folds in L. elenae are distinct;

those of L. latinasus are indistinct or absent. Leptodactylus

latinasus has a mid-dorsal irregular mark, usually reddish

or copper in color (in life); this marking is absent in L. ele-

nae. Leptodactylus latinasus and L. caatingae have consider-

able morphological and color pattern overlap. However,

L. latinasus and L. caatingae have allopatric distributions

and the advertisement calls of L. latinasus are not pulsed

and have higher dominant frequencies (3,000–3,780 Hz)

than the calls of L. caatingae that are pulsed and have low-

er dominant frequencies (940–1,620 Hz).



mula 2(2)/3(1), P1 gap very narrow; tail mottled (Cei,

1980:326, 329; Borteiro and Kolenc, 2007:3–6).


quency 3,100–4,000 Hz; call duration 0.11–0.20 s; each

call a single pulse; rising frequency modulations through-

out call; call rate 2.3/s; no harmonic structure (Heyer,

1978:58–59) (Fig. 36).

Distribution. Argentina, Bolivia, Brazil, Paraguay, and

Uruguay (Fig. 37).

Leptodactylus longirostris Boulenger, 1882

(Plate 3E)

Leptodactylus longirostris Boulenger, 1882:240. Type local-

ity: “Santarem,” Pará, Brazil; see Crombie and Heyer,

1983:291–296, for discussion of type locality. Lecto-

type: BMNH 76.5.26.4, female, designated by Heyer,

1978:32.

Etymology. From Latin longus (long) and rostrum (snout).

Adult morphology. Small to moderate size, female SVL

33.3–45.6 mm (X = 40.0 mm), male SVL 33.1–44.2 mm


thumb spines and chest spines; light upper lip stripe

either indistinct (60% of specimens) or distinct (40%);

dorsal folds present or absent; dorsolateral folds pres-

ent; lateral folds interrupted or absent; posterior thigh

with distinct light stripe (80%) or indistinct (20%); up-

per shank barred; belly uniform light to weakly speck-

led in area next to arm insertion; toes without lat-

eral fringes (Heyer, 1978:61–64; Crombie and Heyer,

1983:293–294).

Similar species. Leptodactylus longirostris occurs in the

Guiana shield region and the Brazilian states of Amazo-

nas, Pará, and Roraima. Similar species within the dis-

tribution of L. longirostris are L. fuscus, L. mystaceus, and

L. poecilochilus. Only individuals of L. longirostris with

light mid-dorsal stripes have dorsal folds; all L. fuscus

have a pair of dorsal folds (individual L. longirostris with

Figure 36. Advertisement call of Leptodactylus latinasus (recording

USNM 19).

Figure 37. Distribution map of Leptodactylus latinasus.




S38


light mid-dorsal stripes are morphologically difficult to

distinguish from L. fuscus). The duration of the adver-

tisement call of L. fuscus ranges from 0.16–0/17 s; the

call duration of L. longirostris ranges from 0.01–0.04 s.

Leptodactylus longirostris lack white tubercles on the

sole of the foot; L. mystaceus have white tubercles on

the sole of the foot. Leptodactylus longirostris have indis-

tinct (60% of specimens) to distinct (40%) light upper

lip stripes; L. poecilochilus lack distinct light lip stripes

but often (67%) have a dark suborbital bar not found in

L. longirostris.


41) 37.0 mm; oral disk anteroventral; tooth row formu-

la 2(2)/3(0,1); tail mottled (Duellman, 1997:24, fig. 20;

Crombie and Heyer, 1983:295–296


quency 940–2,500 or 1,150–3,000 or 1,500–3,600 Hz;

call duration 0.04–0.08 s; calls typically of a single pulse;

rising frequency modulations throughout call; call rate

1.4–2.0/s; harmonic structure apparently present or ab-

sent (Crombie and Heyer, 1983:294–295; Lescure and

Marty, 2000:372) (Fig. 38).

Distribution. Guiana Shield region and adjacent Brazil

(Fig. 39).

Leptodactylus marambaiae Izecksohn, 1976

(Plate 3F)

Leptodactylus marambaiae Izecksohn, 1976:528. Type lo-

cality: “Restinga da Marambaia, Estado do Rio de

Janeiro, vivendo nas proximidades do mar [aproxi-

madamente 23°03’S, 43°38~ ],” Brazil. Holotype: EI

4123, male.

Etymology. Named for the island, Restinga da Maram-

baia, the only known locality for the species.


40.0–41.3 mm (X = 40.6 mm), male SVL 35.8–39.3 mm

(X = 37.0 mm); males lack thumb spines and chest spines;

light upper lip stripe distinct; a pair of well-defined dor-

sal folds; a pair of well-defined dorsolateral folds; a pair

of lateral folds; light stripe on posterior thigh usually

distinct; upper shank with light longitudinal pin stripes;

belly speckled; toes without lateral fringes (Izecksohn,

1976:528; Heyer, 1978:64).

Similar species. Leptodactylus marambaiae occurs only on

the island of Restinga da Marambaia; there are no other

similar species occurring on the island. There is only one

similar species in the State of Rio de Janeiro, Leptodacty-

lus fuscus. Leptodactylus marambaiae has light, narrow lon-

gitudinal stripes on the upper shank; L. fuscus lacks such

light upper shank stripes.


Figure 38. Advertisement of Leptodactylus longirostris (recording

USNM 53).

Figure 39. Distribution map of Leptodactylus longirostris.

Figure 40. Advertisement of Leptodactylus marambaiae (recording

USNM 329).




S39



quency 3,000–3,700 Hz; call duration about 2 s; about 17

notes per call; note duration about 0.02 s; rising frequen-

cy modulations throughout call; no harmonic structure

(Heyer, 1978:64–65) (Fig. 40).

Distribution. Restinga da Marambaia, State of Rio de Ja-

neiro (Fig. 41).

Leptodactylus mystaceus (Spix, 1824) (Plate 4A)

Rana mystacea Spix, 1824:27. Type locality: “ad Bahiam

[now Salvador, Bahia] in aqua fluviatili; differt ab

illa prope flumen Solimoens,” Brazil; restricted to

Solimões (Brazil) by lectotype designation of Méhe-

ly, 1904:219; restricted in error to “Salvador, Bahia”,

Brazil, by Bokermann, 1966:90. Syntypes: Not spe-

cifically stated, but including animals figured on

pl. 3, figs. 1 and 3 in the original publication, ZSM

2504/0 and 2505/0 (lost after 1955 according to

Hoogmoed and Gruber, 1983:357); specimen fig-

ured in pl. 3, fig. 1 designated lectotype by implica-

tion of Peters, 1872a:196–227; Méhelÿ, 1904:219

designated ZSM 2504/0 as lectotype.

Leptodactylus mystaceus: Fitzinger, 1826:64; Méhelÿ,

1904:219.

Cystignathus mystaceus: Wagler, 1830:203; Hensel,

1867:125.

Leptodactylus (Cavicola) mystaceus: Lutz, 1930:22.

Leptodactylus amazonicus Heyer, 1978:38. Type local-

ity: “Ecuador; Napo Province, Limoncocha, 00°24’S,

76°37’W, elevation 260 m.” Holotype: LACM 92111,

by original designation.). Synonymy by Heyer,

1983:270.

Etymology. From the Greek mystax, mystakos, upper lip,

mustache, referring to the obvious light facial stripe.


56.1 mm (X = 50.1 mm), male SVL 42.4–52.2 mm

(X = 47.4 mm); adult male snout spatulate; males lacking

thumb spines and chest spines; light upper lip stripe distinct

(56% of specimens) or indistinct (44%); dorsal folds absent;

dorsolateral folds distinct, complete; lateral folds absent; pos-

terior thighs with light, transverse stripe (93%); upper shank

barred; belly uniform light to small melanophore blotches

scattered across anterior belly and extending centrally; toes

without lateral fringes (Heyer, 1978:38–44, as L. amazonicus).

Similar species. Leptodactylus mystaceus has a broad dis-

tribution in the Amazon basin and extending as far as the

interior portions of the Brazilian states of Minas Gerais

and São Paulo, as well as the northern Atlantic Forests

of Brazil. Similar species lacking toe fringing that occur

with L. mystaceus are L. didymus, L. fuscus, L. gracilis, and

L. longirostris. Leptodactylus didymus and L. mystaceus are

morphologically indistinguishable. The advertisement

Figure 42. Advertisement of Leptodactylus mystaceus (recording USNM

22).

Figure 43. Distribution map of Leptodactylus mystaceus.

Figure 41. Distribution map of Leptodactylus marambaiae.




S40


call of L. mystaceus is pulsed; the call of L. didymus is un-

pulsed. Leptodactylus fuscus and L. gracilis have a pair of

dorsal folds; L. mystaceus lacks dorsal folds. Leptodactylus

mystaceus has light tubercles on the sole of the foot; L. lon-

girostris lacks tubercles on the sole of the foot.



2(2)/3(1); tail mottled (Heyer, 1978:41–42).


quency 700–1,400 Hz; note duration 0.2 s; notes pulsed;

rising frequency modulations throughout call; call = note

rate 1.8/s; no harmonic structure (Heyer, 1978:41, 43;

Heyer et al., 1996a:7–31) (Fig. 42).

Distribution. Amazonia, extending into interior portions

of the Brazilian states of Minas Gerais and São Paulo and

in mesic enclaves in northeastern Brazil as well as north-

ern portions of the Atlantic Forests of Brazil (Fig. 43).

Leptodactylus mystacinus (Burmeister, 1861)

(Plate 4B)

Cystignathus mystacinus Burmeister, 1861:532. Type lo-

cality: “Rozario,” Argentina. Holotype: MLU unnum-

bered male according to Heyer, 1978:68.

Cystignathus labialis Cope, 1877:90. Type locality: “The

precise habitat of this species is at present uncer-

tain. It is probably a part of Sumichrast’s Mexican

collection.” Other specimens Cope described in the

same paper had the following statement: “Habitat

unknown, but supposed to be the Argentine Con-

federation” (page 92). It is likely that the specimens

Cope described as C. labialis were from Argentina.

Type locality restricted in error by Smith and Tay-

lor, 1950:350, to “Potrero Viejo,” Veracruz; rendered

as “probably Tehuantepec, Oaxaca, Mexico” by Co-

chran, 1961:40. Previous statements and restric-

tions of type locality are in error according to Heyer,

2002:321, who made the synonymy, following Heyer,

1978:84. Types: Kellogg, 1932:84 considered USNM

31300–31305 to be syntypes of C. labialis. Cochran,

1961:40, however, considered USNM 31302 to be

the holotype and the other specimens paratypes,

thus a lectotype designation by implication.

Leptodactylus labialis: Brocchi, 1881–1883:20.

Leptodactylus mystacinus: Boulenger, 1882:244.

Leptodactylus (Cavicola) mystacinus: Lutz, 1930:22.

Etymology. From the Greek mystax, upper lip, in allusion

to the striking light upper lip stripe.


67.1 mm (X = 57.4 mm), male SVL 43.6–65.0 mm

(X = 54.1 mm); adult male snout spatulate; males

lacking thumb spines and chest spines; light upper

lip stripe usually distinct (86% of specimens); dorsal

folds absent; usually a pair of distinct dorsolateral

folds; dorsum between the dorsolateral folds without

markings or pattern; lateral folds interrupted or ab-

sent; light posterior thigh stripe usually absent (94%

of specimens), rarely indistinct (6%); upper shank

barred; belly lightly mottled; toes without lateral

fringes (Heyer, 1978:65–68; Heyer et al., 2003:1; Saz-

ima 1975:7–11).

Figure 44. Advertisement of Leptodactylus mystacinus (recording USNM

16).

Figure 45. Distribution map of Leptodactylus mystacinus.




S41


Similar species. Leptodactylus mystacinus occurs in Boliv-

ia, Argentina, central, eastern, and southern Brazil, Para-

guay, and Uruguay. The only similar species that occurs

with L. mystacinus (with no light thigh stripe and distinct

white tubercles on the posterior surface of the tarsus) is

L. bufonius. Leptodactylus mystacinus has distinct dorsolat-

eral folds; dorsolateral folds in L. bufonius are indistinct

or absent.



mula 2(1)/3(1); tail mottled (Heyer et al., 2003:1–2;

Sazima, 1975:32–34; note that Cei’s, 1980, illustration

on page 332 is likely not of L. mystacinus). Langone and

de Sá (2005) reviewed available descriptions for the

species.


cy between 2,050–2,500 Hz; call duration 0.04–0.06 s;

call a single note; call lacking or with negligible amplitude

modulation; call rate 250–400/min; harmonic structure

present or absent (Heyer et al., 2003:2–3) (Fig. 44).

Distribution. Argentina, Bolivia, central- eastern- and

southern Brazil, Paraguay, and Uruguay (Fig. 45).

Leptodactylus notoaktites Heyer, 1978 (Plate 4C)

Leptodactylus notoaktites Heyer, 1978:68. Type local-

ity: “Brasil: São Paulo, Iporanga.” Holotype: MZUSP

25428, female.

Etymology. From the Greek notos, south, and aktites,

coast dweller, in reference to the distribution of the

species.


55.8 mm (X = 48.0 mm), male SVL 42.5–54.2 mm

(X = 47.5 mm); male snout weakly spatulate; males lack-

ing thumb spines; males lacking chest spines; light upper

lip stripe from tip of snout to jaw commissure; a pair of

dorsal folds only in individuals with a light mid-dorsal

stripe; dorsolateral folds distinct; lateral folds interrupt-

ed; posterior thigh with light stripe; upper shank barred;

belly uniform light to having small spots on lateral and

anterior portions of belly (Heyer, 1978:68–69).

Similar species. Leptodactylus notoaktites occurs in the

Atlantic Forest Morphoclimatic Domain in the Brazil-

ian states of Paraná, Santa Catarina, and São Paulo. The

only other similar species that occurs in the more inte-

rior regions of the State of São Paulo is L. mystaceus. Only

individual L. notoaktites with a light mid-dorsal stripe

also have a pair of dorsal folds; no L. mystaceus have

a pair of dorsal folds or a light mid-dorsal stripe. Some

L. notoaktites have a smooth sole of the foot; all L. mysta-

ceus have white tubercles on the sole of the foot.



2(2)/3; tail finely speckled with dark melanophores (de Sá

et al., 2007b:70).


quency modulated between 567–631 Hz at beginning

of call, rising to 1,700–1,788 Hz at end of call; call du-

ration 0.086–0.096 s; each call a single partially pulsed

note; rising frequencies throughout most of call with

short plateaus at beginning and end of call; call rate

0.7 calls/s; calls with pronounced harmonic structure

(Fig. 46).

Distribution. Atlantic forests in the Brazilian states of

Paraná, Santa Catarina, and São Paulo (Fig. 47).

Figure 46. Advertisement of Leptodactylus notoaktites (recording USNM

10).

Figure 47. Distribution map of Leptodactylus notoaktites.




S42


Leptodactylus oreomantis Carvalho, Fortes, Pezzuti,

2013

Leptodactylus oreomantis Carvalho, Fortes, Pezzuti,

2013:350. Type locality: Brazil, Bahia, Municipality

of Rio de Contas, Serra das Almas, Vale do Queiroz.

Holotype: UFMG 3825, adult male.

Etymology. From the Greek oreos, mountain + man-

tis prophet, but also used to refer to frogs as weather

forecasters.



snout pointed, weakly spatulate; body slender; males with-

out thumb and chest spines; irregular brown upper lip stripe

overlaid with a white band; dorsal folds present; continu-

ous, sinuous dorsolateral folds; lateral folds present; light

stripe on posterior surface of thigh present; upper surfaces

of thigh and shank uniformly barred; belly uniform light;

toes lacking expanded tips, fringing, or webbing.

Similar species. Leptodactylus oreomantis occurs in Cam-

po Rupestre areas from Chapada Diamantina. Morpho-

logical similar species are L. furnarius and L. tapiti that

have peep-like advertisement calls whereas L. oreomantis

has a trill-like call.



quency between 2,700–3,100 Hz; call = note duration

0.74–5.09 s; non-pulsed notes; rising frequency modula-

tions throughout call; call rate 7–13/min; harmonic struc-

ture present (Carvalho et al. 2013).

Distribution. Known only from the type locality in the

State of Bahia, Brazil.

Leptodactylus plaumanni Ahl, 1936 (Plate 4D)

Leptodactylus plaumanni Ahl, 1936:389. Type locality: “Nova

Teutonia, [Santa Catarina State], Brasilien,” 22°17’S,

52°20’W. Holotype: Originally in Deutsch Kolonial and

Uebersee Museum, Bremen, now SMF 22469, male.

Leptodactylus geminus Barrio, 1973:199. Type locality:

“Bernardo de Irigoyen, Misiones, Argentina.” Holo-

type: CHINM 5860, by original designation, now in

MACN as MACN 5860, sex uncertain (the jar label

indicates the specimen is a male, but WRH could not

detect vocal slits and he considers the specimen to

be a female). Synonymy by Kwet et al., 2001:56.

Etymology. Ernst Ahl named Leptodactylus plaumanni

for Fritz Plaumann, who lived and collected around Nova

Teutonia (now Seara), Santa Catarina, Brazil. Plaumann

collected insects primarily but also sent frogs to Dr. Ahl

for incorporation in the German collection curated by Dr.

Ahl.

Adult morphology. Moderate size, female SVL 40–

46 mm, male SVL 35–42 mm (data from Kwet and Di-

Bernardo, 1999:66); male snout calloused, not spatulate;

males lacking thumb spines and chest spines; light upper

lip stripe distinct; a pair of distinct dorsal folds; a pair of

distinct dorsolateral folds; a pair of distinct lateral folds;

Figure 48. Advertisement of Leptodactylus plaumanni (recording USNM

226).

Figure 49. Distribution map of Leptodactylus plaumanni.




S43


posterior thigh with light stripe; upper shank with nar-

row longitudinal light stripes; belly uniform light; toes

without lateral fringes (Barrio, 1973:199–206 [as L. gemi-

nus], Kwet and Di-Bernardo, 1999:66–67).

Similar species. Leptodactylus plaumanni occurs in

the Province of Misiones, Argentina and the states of

Rio Grande do Sul and Santa Catarina, Brazil. The only

other species that occurs in this region that has narrow

light longitudinal stripes on the upper shanks is L. graci-

lis. There are no morphological features that differenti-

ate L. plaumanni from L. gracilis. The advertisement call

rate of L. plaumanni is 13–23 calls/s; that of L. gracilis is

3–4 calls/s.

Larval morphology. The larva has not been described. A

recent examination of larvae at the Herpetological collec-

tion of the Museu de Ciencias e Tecnologia, PUCRS, dis-

covered a single tadpole with catalog number MCP3913

from Potreiro Vivo, Sao Francisco de Paula, Rio Grande do

Sul, Brazil. Email communication (November 11, 2013)

with Dr. Mirco Solé informed that this specimen is from

a clutch laid by adults of L. plaumanni within one of his

experimental enclosures (1 m2). The larva has a maxi-

mum total length (Gosner 26) 32 mm; oral disk antero-

ventral; with ventrolateral folds on each side; tooth row

formula 2(2)/3(2); tail light-brown without markings;

fins transparent.


quency 2,700–3,100 Hz; note duration 0.02–0.03 s; notes

of 1–3 pulses; rising frequency modulation throughout

call; no harmonic structure (Barrio, 1973:199–206; Car-

doso, 1985:87–90) (Fig. 48).

Distribution. Argentina (Misiones) and southern Brazil

(Rio Grande do Sul, Paraná, and Santa Catarina) (Fig. 49).

Leptodactylus poecilochilus (Cope, 1862) (Plate 4E)

Cystignathus poecilochilus Cope, 1862:156. Type locality:

“Near Turbo, [Antioquia,] New Granada [= Colom-

bia].” Syntype: “Mus. Smithsonian [USNM], [No.

4347] Acad., Philadelphia,” male. Cope apparently

had two specimens in hand that he considered as

types. One of the types was clearly designated as be-

longing in the USNM; the other specimen was pre-

sumably deposited in the ANSP but seemingly has

since been lost. Cochran, 1961:40, reported USNM

“4347a” to be the holotype, but the specimen tag on

the USNM type does not bear an “a.”

Leptodactylus poecilochilus: Boulenger, 1882:343.

Leptodactylus quadrivittatus Cope, 1894 “1893”:339. Type

locality: “Buenos Ayres” [= Buenos Aires], Cantón

de Buenas Aires, Provincia de Puntarenas, Costa

Rica (for comments on the type locality see Savage,

1974:82). Holotype: Originally No. 365 in Museo

Nacional de Costa Rica; now lost according to Dunn,

1940:106. Synonymy by Dunn, 1940:106; Heyer,

1970b “1968”:182; Heyer, 1978:33.

Leptodactylus maculilabris Boulenger, 1896:404–405.

Type locality: “Bebedero, [Cantón de Cañas, Prov-

ince of Guanacaste,] Costa Rica” (for comments on

the type locality see Savage, 1974:78). Holotype:

BMNH 94.11.15.27. Synonymy by Dunn, 1940:106;

Heyer, 1970b “1968”:182; Heyer, 1978:33.

Leptodactylus diptychus Boulenger, 1918:431. Type lo-

cality: “Andes of Venezuela.” Holotype: BMNH

94.8.31.11, female.) Synonymy by Heyer, 1978:34.

Leptodactylus poecilochilus poecilochilus: Rivero, 1961:43.

Leptodactylus poecilochilus dyptichus: Rivero, 1961:42. In-

correct subsequent spelling for diptychus.

Etymology. From the Greek poikilos, variegated, and chei-

los, lip.


54.1 mm (X = 46.2 mm), male SVL 39.0–48.7 mm

(X = 44.6 mm); adult male snout spatulate; males lacking

thumb spines and chest spines; light upper lip stripe in-

distinct; a pair of dorsal folds only in individuals with a

light mid-dorsal stripe; distinct pair of dorsolateral folds;

lateral folds complete; posterior thigh light stripe usually

distinct (77% of specimens), sometimes indistinct (21%),

rarely absent (2%); upper shank barred; belly usually light

or with light speckling; toes without lateral fringes (Hey-

er, 1970b “1968”:182–184, 1978:69–71).

Similar species. Species that lack toe fringes and co-occur

with Leptodactylus poecilochilus are L. fragilis and L. fuscus.

Leptodactylus poecilochilus have a pair of distinct dorsolat-

eral folds; L. fragilis have indistinct dorsolateral folds. Only

specimens of L. poecilochilus that have a broad mid-dorsal

light stripe also have a pair of dorsal folds, most lack scat-

tered dorsal blotches, and most (67% of specimens) have

a dark sub-orbital bar; all L. fuscus have a pair of dorsal

folds, scattered dorsal blotches, and no suborbital bar.


41) 37 mm; oral disk anteroventral; tooth row formula

2(2)/3[1]; tail mottled (Heyer, 1970b “1968”:183–184,

195–199).


quency 350–550 Hz (Panamá) or 700–1,300 Hz (Costa

Rica); call/note duration 0.055–0.080 s; call not pulsed;

rising frequency modulations throughout call; call rate

1.7/s; harmonic structure present or absent (Fouquette,

1960:205, 207–209 [as L. quadrivittatus], Heyer, 1978:69)

(Fig. 50).




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Distribution. Lowlands of Costa Rica to north coastal

South America as far as Venezuela (Fig. 51).

Leptodactylus sertanejo Giaretta and Costa, 2007

(Plate 4F)

Leptodactylus sertanejo Giaretta and Costa, 2007:3. Type

locality: “Clube de Caça e Pesca Itororó de Uberlân-

dia (around 19°00’00”S, 48°18’53”W, 850 m asl),

municipality of Uberlândia, State of Minas Gerais,

Brazil.” Holotype: ZUEC 13657, adult male.

Etymology. “The specific name ‘sertanejo’ is a Portuguese

word to those people who live in the wilderness, far from

civilization. It also can refer to the Brazilian country mu-

sic, generally performed by duets. We use it as a noun in

apposition to make reference to our preferred way of life

which includes a lot of outdoor activities, including field

works, sometimes listening to traditional Brazilian mu-

sic.” (Giaretta and Costa, 2007:9).

Adult morphology. Moderate size, female SVL

X = 54.3 mm (1.4 SD), male SVL X = 51.0 mm (1.7 SD);

adult male snout not spatulate (based on illustration in Gi-

aretta and Costa, 2007:7, fig. 4); males lack thumb spines

and chest spines; distinct light upper lip stripe; distinct

pair of dorsal folds; distinct pair of dorsolateral folds; dis-

tinct pair of lateral folds; posterior thigh with light stripe

(based on similarity with L. jolyi); upper shank with a light

longitudinal pin stripe; belly and throat cream; toes with-

out lateral fringes (Giaretta and Costa, 2007:1–10).

Similar species. Leptodactylus sertanejo is very similar to

L. jolyi. At present, the only verified locality for L. sertane-

jo is the Municipality of Uberlândia, Minas Gerais, Brazil,

in the Cerrado Morphoclimatic Domain of Brazil. Giaretta

and Costa (2007) indicated that the type locality of L. jolyi

was degraded Atlantic Forest Morphoclimatic Domain;

Giaretta and Costa (2007) predicted that frogs currently

identified as L. jolyi from Cerrado habitats will prove to be

L. sertanejo. Leptodactylus jolyi and L. sertanejo cannot be

reliably differentiated from each other morphologically.

The advertisement call rate of L. jolyi is 0.1–0.3/s; that of

L. sertanejo is 0.02–0.3/s; the call of L. jolyi is longer (mode

= 0.04 ms) than that of L. sertanejo (mode = 0.02 ms).

Figure 50. Advertisement of Leptodactylus poecilochilus.

Figure 51. Distribution map of Leptodactylus poecilochilus.

Figure 52. Advertisement of Leptodactylus sertanejo.

Figure 53. Distribution map of Leptodactylus sertanejo.




S45



Advertisement call. Dominant frequency 2,000–

2,400 Hz; call duration 0.02–0.03 s; call (= note) single or

double-pulsed; rising frequency modulations throughout

call; call rate 1–18/min.; no harmonic structure (Giaretta

and Costa 2007:1–10) (Fig. 52).

Distribution. Currently known from the Municipality of

Uberlândia, Minas Gerais; predicted to occur more broad-

ly in the Cerrado Morphoclimatic Domain (Fig. 53).

Leptodactylus spixi Heyer, 1983 (Plate 5A)

Leptodactylus spixi Heyer, 1983:270. Type locality: “Brazil:

Rio de Janeiro; Saco de São Francisco, Niteroi.” Ho-

lotype: USNM 96409, adult male.

Etymology. Named for Johann Baptist von Spix, one of

the earliest naturalists to collect and report on Brazilian

amphibians and reptiles.


48.6 mm (X = 43.8 mm), male SVL 38.8–47.1 mm

(X = 42.6 mm); adult male snout variable, spatulate in

some males, rounded in others; males lack thumb spines

and chest spines; light upper lip stripe usually distinct

(79% of specimens); dorsal folds present only in individu-

als with a light mid-dorsal stripe; distinct pair of dorso-

lateral folds; lateral folds interrupted or absent; posterior

thigh with light stripe; upper shank barred; belly without

pattern or with small spots on lateral and anterior bel-

ly; toes without lateral fringes (Heyer, 1978:64–65 [as

L. mystaceus]; Heyer, 1983:270–272).

Similar species. Leptodactylus spixi occurs in the At-

lantic Forests of the Brazilian states of Bahia, Espírito

Santo, and Rio de Janeiro. It is unclear whether there is

distributional overlap of L. spixi with L. mystaceus in Ba-

hia or more northern coastal Brazilian states (Alagoas,

Pernambuco, Rio Grande do Sul, Sergipe). In addition

to L. mystaceus, other similar species are L. fuscus and

L. marambaiae; all of these species lack toe fringes and

have light transverse stripes on the posterior thighs.

Only individuals of L. spixi that have a median light

dorsal stripe have a pair of dorsal folds and all L. spixi

have white tubercles on the dorsal shank surface; all

specimens of L. fuscus have a pair of dorsal folds and

lack white tubercles on the dorsal shank surface. Lep-

todactylus spixi lacks a narrow, light longitudinal stripe

on the upper surface of the shank; L. marambaiae has a

light longitudinal stripe on the upper shank. Leptodacty-

lus spixi has white tubercles on the upper shank surface;

L. mystaceus has no white tubercles on the upper shank

surface.



2(2)/3; tail mottled (Bilate et al., 2007 “2006”:238–240).


quency 1,500–1,722 and 1,981–2,067 Hz; call duration

120 ± 10 ms; call consisting of a single unpulsed note; ris-

ing frequency modulations through most of call; call rate

80–97/min; call with pronounced harmonic structure (Bi-

late et al., 2007 “2006”:237–238) (Fig. 54).

Distribution. Atlantic forests in the Brazilian states of

Bahia, Espírito Santo, and Rio de Janeiro (Fig. 55).

Leptodactylus syphax Bokermann, 1969 (Plate 5B)

Leptodactylus syphax Bokermann, 1969:13. Type locality:

“São Vicente [Gustavo Dutra], Cuiabá, 600 m, Mato

Grosso, Brasil.” Holotype: MZUSP 73851, originally

WCAB 16141, adult male.

Figure 54. Advertisement of Leptodactylus spixi.

Figure 55. Distribution map of Leptodactylus spixi.




S46


Etymology. From the Greek syphax (sweet new wine) in

allusion to the bright red color in life of the groin, belly,

and ventral surfaces of the thighs and shanks occurring in

some, but not all, specimens.


89.8 mm (X = 78.8 mm), male SVL 57.5–83.4 mm


males with a pair of large, black, sharp thumb spines and

a pair of black sharp chest spines; light upper lip stripe

absent; dorsal folds absent; dorsolateral folds absent; lat-

eral folds absent or largely interrupted; posterior thigh

without a light stripe; upper shank barred; belly lightly

to moderately mottled with light gray or brown mark-

ings; lateral surfaces of toes smooth or weakly ridged (not

fringed) (Heyer et al., 2010a:1).

Similar species. Leptodactylus syphax occurs in open

habitats, characteristically rocky outcrops, in Bolivia (De-

partment of Santa Cruz), Brazil (States of Ceará, Goiás,

Mato Grosso, Mato Grosso do Sul, Minas Gerais, Paraiba,

Piauí, São Paulo, Tocantins, and Distrito Federal), and

Paraguay (Departments of Concepción, La Cordillera).

Other species that occur with L. syphax that lack dorso-

lateral folds and toe fringes are L. bufonius, L. labyrinthi-

cus, L. laticeps, and L. troglodytes. Leptodactylus syphax is

larger than L. bufonius (male SVL 45–49 mm, female SVL

49–62 mm SVL) and male L. syphax have thumb and chest

spines; male L. bufonius lack thumb and chest spines. Lep-

todactylus syphax is smaller (maximum 90 mm SVL) than

L. labyrinthicus (minimum 117 mm SVL) and L. syphax has

no dorsolateral folds; most L. labyrinthicus have a distinct

short pair of dorsolateral folds extending varying distanc-

es from behind the eye to the sacrum. The dorsal pattern

of L. syphax is muted; the dorsal pattern of L. laticeps is vi-

sually arresting with an aposematic, contrasting dark and

light tile-like pattern that is bright yellow, red, and black

in life. Leptodactylus syphax is larger than L. troglodytes

(male SVL 45–53 mm, female SVL 45–53 mm SVL) and

male L. syphax have thumb and chest spines; L. troglodytes

males have neither thumb nor chest spines. Leptodactylus

syphax lacks a pseudo-odontoid on lower jaw; L. troglo-

dytes has a pseudo-odonotid on lower jaw.


41) 43.9 mm; oral disk anteroventral, tooth row formula

2(2)/3(1); tail mottled (Heyer et al., 2010a:1–2).


cy 1,310–1,330, 1,640–1,680, or 1,800–1,850 Hz; call du-

ration 53–64 ms; calls with 2–3 pulses; rising frequency

modulations throughout call; call rate 48–90/min; har-

monic structure present (Heyer et al., 2010a:2) (Fig. 56).

Distribution. Leptodactylus syphax occurs in open habi-

tats, usually rocky outcrops, in Bolivia, Brazil, and Para-

guay (Fig. 57).

Leptodactylus tapiti Sazima and Bokermann, 1978

(Plate 5C)

Leptodactylus tapiti Sazima and Bokermann, 1978:910.

Type locality: “Chapada dos Veadeiros, [1800 m],

Alto Paraíso de Goiás, Goiás, Brasil.” Holotype:

MZUSP 73680, originally WCAB 47622, adult male.

Etymology. Sazima and Bokermann (1978) did not provide

an etymology for their new species Leptodactylus tapiti. “Ta-

piti” is an indigenous name for rabbit, presumably named as

for their other new species L. cunicularius, which excavates

the incubating chamber in a manner similar to rabbits.


(X = 38.3 mm), male SVL 29.8–33.4 mm (X = 31.6 mm); Figure 56. Advertisement of Leptodactylus syphax (recording USNM

319).

Figure 57. Distribution map of Leptodactylus syphax.




S47


adult male snout spatulate; males lacking thumb spines

and chest spines; uniform or irregular light upper lip

stripe; dorsal folds present; continuous, sinuous dorso-

lateral folds; lateral folds present; posterior thigh with a

light stripe or a line of small light spots; upper shank with

interrupted, narrow, longitudinal folds highlighted by

small, light dots and lines; belly uniform light; toes with-

out lateral fringes (Sazima and Bokermann, 1978:910).

Similar species. Other species without fringed toes and

complete, interrupted, or no light stripes on the poste-

rior thigh in some or possibly all specimens occurring

with L. tapiti are L. fuscus, L. mystaceus, and L. mystacinus.

Leptodactylus tapiti have interrupted narrow longitudinal

folds on the upper shanks; L. fuscus, L. mystaceus, and

L. mystacinus lack any folds or interrupted fold-like struc-

tures on the upper shank.

Larval morphology. Maximum total length (Gos-

ner 38) 41.0 mm; oral disk anteroventral; tooth row

formula 2(2)/3(1); tail mottled (Sazima and Bokermann,

1978:909, 911).


quency 3,273–3,617 Hz; call duration 31.5–43.9 ms; calls

with 2–3 pulses;; call rate 3.0 ± 1.5 notes per second; call

without harmonics and an ascendant modulation fre-

quency (Brandão et al., 2013) (Fig. 58).

Distribution. Chapada dos Veadeiros (1800 m), Alto

Paraíso, Goiás, Brazil (Sazima and Bokermann, 1978:910)

(Fig. 59).

Leptodactylus troglodytes Lutz, 1926a (Plate 5D)

Leptodactylus troglodytes Lutz, 1926a:149. Type locality:

“Pernambuco,” Brazil. Holotype: AL-MN 816, adult

female.

Leptodactylus (Cavicola) troglodytes: Lutz, 1930:2, 22.

Etymology. From the Greek trōglē (hole made by gnaw-

ing) and dytēs (burrower), one who creeps into holes.


44.9–52.7 mm (X = 50.0 mm), male SVL 45.5–52.8 mm

(X = 48.3 mm); adult male snout spatulate; males lack thumb

spines and chest spines; light upper lip stripe absent; dorsal

folds absent; dorsolateral folds indistinct, usually absent;

lateral folds interrupted or absent; posterior thigh without

light stripe; upper shank barred; belly uniform light; toes

without lateral fringes (Heyer, 1978:71–73).

Similar species. Leptodactylus troglodytes occurs from the

state of Minas Gerais in southeast to northeast Brazil (States

of Piauí, Ceará, Rio Grande do Norte, Paraíba, Pernambuco,

Alagoas, Sergipe, and Bahia). Within the distribution of

L. troglodytes the only other species that lacks toe fringes,

lacks a light thigh stripe, and has distinct white tubercles

on the posterior surface of the tarsus is L. mystacinus. Lep-

todactylus troglodytes has either indistinct or (usually) no

dorsolateral folds; L. mystacinus has distinct, continuous

dorsolateral folds. Leptodactylus troglodytes is unique in the

genus in having a pseudo-odontoid on the lower jaw.



mula 2(2)/2–3[1]; tail mottled (Cascon and Peixoto,

1985:361–364).


quency 3,144 Hz with a frequency modulation range of

517–603 Hz; call duration 364–576 ms; call of a single

unpulsed note; rising frequency modulations throughout

call = note; call rate 56–80/min; no harmonic structure

(Kokubum et al., 2009:120–123) (Fig. 60).

Figure 58. Advertisement of Leptodactylus tapiti.

Figure 59. Distribution map of Leptodactylus tapiti.




S48


Distribution. Minas Gerais State in southeast to North-

east Brazil (Fig. 61).

Leptodactylus ventrimaculatus Boulenger, 1902

(Plate 5E)

Leptodactylus ventrimaculatus Boulenger, 1902:53. Type

locality: “Bulún [Pulún], 160 feet,” Esmeraldas Prov-

ince, Ecuador. Syntypes: BMNH 1947.2.17.78–80 [3

specimens], BMNH 1947.2.17.78 designated lecto-

type by Heyer and Peters, 1971:166, adult female.

Etymology. From the Latin venter (belly) and maculatus

(spotted, variegated, full of spots).


63.2 mm (X = 53.2 mm), male SVL 43.5–60.3 mm

(X = 51.4 mm); adult male snout not spatulate; males

lacking thumb spines and chest spines; light upper lip

stripe absent; dorsal folds absent; dorsolateral folds usu-

ally present; lateral folds absent; light stripe on posterior

thigh almost always absent (97% of specimens), rarely in-

distinct (3%); upper shank barred; belly slightly to heavily

mottled; toes without lateral fringes (Heyer, 1978:73–74).

Similar species. Leptodactylus ventrimaculatus occurs in

the Chocó of Colombia and adjacent coastal rainforests in

Ecuador. The only species that lack a distinct light posterior

thigh stripe and lack toe fringes that co-occur with L. ven-

trimaculatus are L. labrosus and L. rhodomerus. Leptodactylus

ventrimaculatus has distinct, scattered, or very few, white

tubercles on the sole of the foot; L. labrosus usually (91% of

specimens) lack white tubercles on the sole of the foot. Lep-

todactylus ventrimaculatus commonly lack flank folds and,

if present, are of moderate size; L. rhodomerus usually have

continuous to interrupted flank folds and are of large size.


Advertisement call. Unknown.

Distribution. Chocó of Colombia and adjacent Ecuador

(Fig. 62).

Leptodactylus pentadactylus species group

Leptodactylus fallax Müller, 1926 (Plate 5F)

Leptodactylus dominicensis Müller, 1923:42. Type local-

ity: “Dominica,” Lesser Antilles. Holotype: ZSM

258/1909, female). Junior homonym of Leptodacty-

lus dominicensis Cochran, 1923.

Figure 60. Advertisement of Leptodactylus troglodytes (recording USNM

318).

Figure 61. Distribution map of Leptodactylus troglodytes.

Figure 62. Distribution map of Leptodactylus ventrimaculatus.




S49


Leptodactylus fallax Müller, 1926:200. Replacement name

for Leptodactylus dominicensis Müller, 1923.

Etymology. The Latin word fallax means deceptive.

Adult morphology. Large, female SVL 129.2–

167.2 mm (X = 148.6 mm), male SVL 121.0–158.7 mm


with one keratinized thumb spine; males lacking chest

spines; light upper lip stripe absent; dorsal folds absent;

dorsolateral folds usually complete; lateral folds complete,

interrupted, or absent; upper shank barred; belly uni-

formly light or with small melanophore blotches scattered

across anterior belly; weak to noticeable lateral ridges on

toes (Kaiser, 1994).

Similar species. Leptodactylus fallax currently occurs on

the islands of Dominica and Monteserrat and is the only

species of Leptodactylus on these islands.

Larval morphology. Maximum total length (Gosner 42)

110.5 mm; oral disk anteriorly positioned; tooth row for-

mula 1/0; tail patternless (no melanophores) (Lescure

and Letellier, 1983:63).


cy 500–1,500 Hz; call duration 0.18–0.20 s; calls pulsed;

rising frequency modulations through most of call with

terminal falling frequency; call rate up to 42/min; no har-

monic structure (Kaiser 1994:1) (Fig. 63).

Distribution. Kaiser (1994:1–2) indicates that only

three Lesser Antillean islands are well documented for

natural occurrence of L. fallax: Dominica, Montser-

rat, and Martinique (L. fallax is now extinct on Marti-

nique). Doubtful island occurrences on Antigua, Gua-

daloupe, and St. Lucia are not supported by voucher

specimens. Attempts to introduce L. fallax on Grena-

da, Martinique, and Puerto Rico have failed (Kaiser,

1994:2) (Fig. 64).

Figure 64. Distribution map of Leptodactylus fallax.

Figure 63. Advertisement call of Leptodactylus fallax (recording USNM

96).

Leptodactylus flavopictus Lutz, 1926a (Plate 6A)

Leptodactylus flavopictus Lutz, 1926a:144. Type locality:

“Mont Serrat na base do Itatiaia,” Rio de Janeiro,

Brazil. Holotype: AL-MN 870, female.

Leptodactylus pachyderma Miranda-Ribeiro, 1926:150.

Type locality: “Ilha Victoria, S[ão] Paulo,” Brazil. Ho-

lotype: MZUSP 351, adult female.

Leptodactylus pentadactylus flavopictus: Cochran,

1955 “1954”:320.

Leptodactylus flavopictus: Heyer, 1979:18.

Etymology. From the Latin flavus, yellow, and pictus,

painted. The color illustration of the venter of L. flavopic-

tus in Lutz 1926a plate 31 displays small yellow spots on

the throat and large yellow blotches on the chest, belly,

and ventral thigh surfaces.


145.0 mm (X = 135.8 mm), male SVL 110.0–135.0 mm


with two keratinized spines on each thumb; adult males

with chest spines; narrow to broad light upper lip stripes;

dorsal folds absent; weak dorsolateral folds; lateral folds

absent; posterior thigh lacking distinct light stripe; upper




S50


shank banded; belly mottled; toes with weak ridges (Hey-

er, 1979:18–20).

Similar species. Leptodactylus flavopictus ranges from the

Brazilian states of Espírito Santo to Santa Catarina. Lep-

todactylus labyrinthicus is the only similar species found in

the general distribution of L. flavopictus. Leptodactylus fla-

vopictus has a light stripe on the upper lip; L. labyrinthicus

lacks a light upper lip stripe.



quency ca. 650 Hz; call duration 0.06–0.09 s; call of single

note/pulse; call without noticeable rising or falling fre-

quency; call rate about 1 call/s; call apparently lacking

harmonic structure (Fig. 65).

Distribution. Atlantic forests from the Brazilian states of

Espírito Santo to Santa Catarina (Fig. 66).

Leptodactylus knudseni Heyer, 1972 (Plate 6B)

Leptodactylus knudseni Heyer, 1972:3. Type locality: Ec-

uador, Napo, Limoncocha. Holotype: LACM 72117,

juvenile female.

Etymology. Named for Dr. Jens W. Knudsen whose men-

toring influenced W.R. Heyer’s pursuit of biology as a

profession.

Adult morphology. Large, female SVL 102.7–154.0 mm


adult snout not spatulate; adult males with a black spine

on each thumb; adult males with a pair of large black chest

spines; upper lip lacking a distinct light stripe; dorsal

folds absent; a pair of dorsolateral folds, usually complete,

sometimes interrupted, originating behind eye; lateral

folds interrupted or absent; posterior thigh lacking a light

stripe, usually dark with small to large light vermicula-

tions or spots; upper shank barred; belly uniform light,

uniform dark, mottled, or dark with small light spots or

vermiculations; toes with or without weak lateral ridges

(Heyer and Heyer, 2006a:1).

Similar species. Leptodactylus knudseni has a broad Ama-

zonian distribution, occurring in the same general areas

as L. labyrinthicus, L. myersi, L. paraensis, L. pentadac-

tylus, and L. stenodema. Juvenile L. knudseni often have

green dorsal coloration in life and solid black posterior

thighs; juvenile L. labyrinthicus, L. myersi, L. paraensis,

and L. pentadactylus are not green in life nor do they have

solid black posterior thigh patterns. The advertisement

calls of L. knudseni are pulsed, the advertisement calls of

L. labyrinthicus are not pulsed. The dorsolateral folds of

L. knudseni are usually complete, the dorsolateral folds in

L. paraensis are interrupted and are often interrupted in

L. labyrinthicus. Sexually active male L. knudseni have a

pair of chest spines; chest spines are lacking in L. myersi

and L. pentadactylus. The dorsolateral folds of L. knudseni

originate behind the eye; the dorsolateral folds of L. steno-

dema originate above the posterior edge of the tympanum.


state 40) 69 mm; oral disk almost terminal; tooth row for-

mula 2(2)/2–3(1); tail mottled (Heyer, 2005:316, Heyer

and Heyer, 2006a:1–2).


quency 340–690 Hz; call duration 0.16–0.43 s; 6–14 puls-

es/call; rising frequency modulations throughout call; call

rate 16–66 calls/min; harmonic structure well-developed

(Heyer, 2005:316; Heyer and Heyer, 2006a:1–2) (Fig. 67).

Distribution. Gran Sabana of Venezuela and adjacent

Lavrado in northern Brazil; mesic, tropical habitats of

Figure 65. Advertisement call of Leptodactylus flavopictus.

Figure 66. Distribution map of Leptodactylus flavopictus.




S51


southern Venezuela south to Bolivia and Brazil extending

eastward from Ecuador, Colombia, Perú, through Guyana,

Suriname, and French Guiana to Trinidad (Fig. 68).

Leptodactylus labyrinthicus (Spix, 1824)

(Plate 6C-D)

Rana labyrinthica Spix, 1824:31. Type locality: “Provincia

Rio de Janeiro,” Brazil. Bokermann, 1966:89 consid-

ered the type locality to be in error and suggested

that it was “Paraiba, já próximo da divisa com São

Paulo.” Holotype: ZSM 2501/0, now lost according

to Hoogmoed and Gruber, 1983:360.

Cystignathus labyrinthicus: Wagler, 1830:203.

Leptodactylus labyrinthicus: Girard, 1853:420.

Pleurodema labyrinthicus: Günther, 1859b “1858”:31.

Gnathophysa labyrinthica: Cope, 1865:112.

Leptodactylus wuchereri Jiménez de la Espada, 1875:68.

Type locality: Imprecise; a rough translation (p. 72)

is that the specimen was collected by Jiménez de la

Espada’s deceased companion, Sr. Amor, somewhere

between Montevideo and Santiago de Chile and that

Jiménez de la Espada did not know in which country

(or countries) the frog was collected, nor anything

about its habits. Holotype: MNCN 1694, female.

Leptodactylus bufo Andersson, 1911:1. Type locality: Pon-

ta Grosso, Paraná, Brazil. Holotype: NRM 1495.

Leptodactylus pentadactylus labyrinthicus: Müller, 1927:276.

Leptodactylus pentadactylus mattogrossensis Schmidt and

Inger, 1951:444. Type locality: “manganese mine,

Urucum de Corumba, Matto Grosso,” Brazil [local-

ity is now in Mato Grosso do Sul]. Holotype: FMNH

9240, adult female.

Leptodactylus pentadactylus matogrossensis: Bokermann,

1966:74.

Etymology. A dictionary definition of labyrinth is “any

intricate or involved enclosure; a maze of paths in a park

or garden; also a representation of such a maze, as in a

print, or as inlaid in a pavement.” Presumably the holo-

type of Rana labyrinthica had a maze-like pattern on the

posterior thighs and/or belly.


166.0 mm (X = 145.0 mm), male SVL 110.6–188.0 mm


males with a single black thumb spine; adult males with

a pair of black chest spines; light upper lip stripe ab-

sent; dorsal folds absent; a pair of dorsolateral folds

usually interrupted from at least midway to full dis-

tance from eye to sacrum, rarely absent; lateral folds

absent; posterior thigh without light longitudinal

stripe, usually dark with a variety of light marks; upper

shank barred; belly pattern usually labyrinthine to im-

maculate; toes with or without lateral ridges (not flex-

ible), vestigial basal web between toes II–III–IV (Heyer,

2005:316–318).

Similar species. Leptodactylus labyrinthicus occurs in

open formation habitats, including Cerado enclaves in

Amazonia. The species most likely to be confused with

L. labyrinthicus are L. knudseni, L. paraensis, and L. vastus.

Most adult L. labyrinthicus have a distinctive labyrinthine

belly pattern; adult L. knudseni lack this pattern. The ad-

vertisement call of L. labyrinthicus is unpulsed; the adver-

tisement call of L. knudseni is pulsed. Leptodactylus par-

aensis is documented only from closed canopy rain forest

in the states of Mato Grosso and Pará, Brazil. There is no

consistent morphological feature that completely distin-

guishes L. labyrinthicus from L. paraensis. Leptodactylus

labyrinthicus is slightly larger (male SVL 117–188 mm, fe-

male SVL 124–166 mm) than L. paraensis (male SVL 94–

170 mm, female SVL 102–154 mm). Heyer et al. (2005)

indicated specimens from Pará previously identified as

Figure 67. Advertisement call of Leptodactylus knudseni (recording

USNM 267).

Figure 68. Distribution map of Leptodactylus knudseni.




S52


L. labyrinthicus or L. knudseni represented a new species

based on genetic data.


80 mm; oral disk almost terminal; tooth row formula

1/2(1); tail mottled (Vizotto, 1967:80–94).


cy ca. 430 Hz; call duration 0.14–0.21 s; calls unpulsed;

slowly rising frequency modulations throughout call;

call rate 35–50/min; harmonic structure present (Heyer,

2005:297, 318) (Fig. 69).

Distribution. Leptodactylus labyrinthicus occurs in open

formation habitats in Argentina (Provinces of Misiones

and Corrientes), Brazil (including Cerrado enclaves in

Amazonia), and Paraguay (Fig. 70).

Leptodactylus lithonaetes Heyer, 1995

Leptodactylus lithonaetes Heyer, 1995:708. Type local-

ity: “Venezuela: Amazonas, SW sector Cerro Yapa-

cana, 600 m, 03°57’N, 67°00’W.” Holotype: AMNH

100656, adult male.

Etymology. From the Greek lithos (stone, rock) and naetes

(inhabitant), in reference to the species association with

rocky outcrops.


78.4 mm (X = 62.8 mm), male SVL 45.3–71.4 mm

(X = 57.0 mm); adult male snout not spatulate; males with

one keratinized thumb spine; males lacking chest spines;

light lip stripe absent; dorsal folds absent; dorsolateral

folds sometimes absent or usually with a series of short

ridges or elongate warts in the shoulder region to series of

ridges from eye to sacrum; lateral folds absent; posterior

thigh without light stripe; upper shank with irregular bars

to irregular spots/blotches; belly uniformly dark to dark

with distinct light spots/flecks; toes without lateral fring-

es (Heyer, 1995:708–711; Heyer and Heyer, 2001:1–3).

Similar species. Leptodactylus lithonaetes occurs in Co-

lombia and Venezuela. The only similar species within

the general distribution of L. lithonaetes having toes not

fringed and indistinct dorsolateral folds is L. rugosus. Lep-

todactylus lithonaetes and L. rugosus differ only in male

secondary sexual characters. Leptodactylus lithonaetes

males have a single black spine on each thumb and a

patch of brown/black tubercles on the chin/throat; some

L. rugosus have a single thumb spine and others have two

spines on each thumb; however, all male L. rugosus lack

chin tubercles.


36.1 mm; oral disk ventral; tooth row formulae 2(2)/3 or

2(2)/3(1); tail mottled (Heyer 1995:709,711).

Advertisement call. Initial dominant (= fundamental)

frequency ca. 600–780 Hz, long portion of call dominant

frequency 2,750–3,200 Hz; call duration 0.62–0.80 s; call

of single pulsed notes; pronounced rising frequencies at

beginning of call, followed by relatively stable frequencies;

calls sporadic (separated by 2 to 20 s; initial portion of

call with pronounced harmonics, most of call apparently

Figure 69. Advertisement call of Leptodactylus labyrinthicus (recording

USNM 229).

Figure 70. Distribution map of Leptodactylus labyrinthicus.




S53


lacking harmonic structure (Heyer and Barrio-Amorós,

2009:282–288) (Fig. 71).

Distribution. Rocky outcrops in Colombian Departments

of Amazonas, Guainía, Vaupés, Vichada and Venezuelan

States of Amazonas, Apure, and Bolívar (Fig. 72).

Leptodactylus myersi Heyer, 1995 (Plate 6E)

Leptodactylus myersi Heyer, 1995:712. Type locality: “Bra-

zil: Roraima; Mucajaí, 02°25’N, 60°55’W”. Holotype:

MZUSP 66089, adult male.

Etymology. Named for Dr. Charles W. Myers for his con-

tributions to Neotropical herpetology in general and for

bringing this new species to W.R. Heyer’s attention in

particular.

Adult morphology. Moderate–large size, female SVL

78.9–112.9 mm (X = 103.2 mm), male SVL 74.2–123.4 mm

(X = 100.5 mm); adult males with one large (rarely small)

keratinized thumb spine; males lack chest spines; upper

lips rarely with a broad light stripe; dorsal folds absent;

dorsolateral folds often absent or interrupted from at

least ¼ to full distance from eye to sacrum; lateral folds

absent; posterior thigh dark with various kinds of light

marks; upper shank barred; belly ranging from dark, with

various kinds of light marks, to almost uniformly light

with very few melanophores; toes without lateral fringes

(Heyer, 1995:710, 712–713; 2005:318–320).

Similar species. Leptodactylus myersi occurs in French

Guiana, Suriname, and adjacent Brazil. The moderate to

large species that co-occur with L. myersi are L. knudseni

and L. pentadactylus. Leptodactylus myersi usually lacks dis-

tinct, complete lateral folds; L. pentadactylus has distinct,

complete lateral folds. Leptodactylus myersi is typically

limited to rocky outcrops in French Guiana, Suriname,

and northeastern Brazil; L. knudseni is widely distributed

throughout the Amazon basin and does not occupy rocky

Figure 71. Advertisement call of Leptodactylus lithonaetes.

Figure 72. Distribution map of f Leptodactylus lithonaetes. Figure 73. Advertisement call of Leptodactylus myersi.

7Figure 74. Distribution map of Leptodactylus myersi.




S54


outcrops. Reproductively active males of L. myersi lack

chest spines; adult males of L. knudseni have chest spines.

Juvenile L. myersi are bright red on their venters and pos-

terior thighs; juvenile L. knudseni lack red coloration and

often have obvious dorsal green coloration.



quency 600–690 Hz; call duration 0.33–0.36 s; each call

with 2–3 pulses; rising frequency modulations through-

out call, from about 330–920 Hz; call rate 36 calls/min;

harmonic structure not apparent (Lescure and Marty,

2000:348, 372) (Fig. 73).

Distribution. Rocky outcrops in French Guiana, Surina-

me, and adjacent Brazil (Fig. 74).

Leptodactylus paraensis Heyer, 2005 (Plate 6F)

Leptodactylus paraensis Heyer, 2005:320. Type local-

ity: “Brazil: Pará, Serra de Kukoinhokren, 07°46’S,

51°57’W.” Holotype: MZUSP 69321, adult male.

Etymology. The species is named after the Brazilian State

of Pará. At the time of description, all specimens were

known only from the State of Pará.



adult male snout not spatulate; male thumb usually with 1

large black spine, rarely with 1 small to tiny spine; breed-

ing males with a pair of chest spines; upper lip without a

light stripe; dorsal folds absent; dorsolateral folds usually

interrupted, extending from eye to ½ distance to sacrum;

lateral folds absent; posterior thigh dark with various

sized light markings; upper shank barred; belly pattern

variable, from uniformly dark to various sized light mark-

ings on a dark background; toes with weak lateral ridges,

not with moveable lateral fringes (Heyer, 2005:320–322).

Similar species. Leptodactylus paraensis has an east-

ern Amazonian distribution (states of Mato Grosso and

Pará) occurring in the same general area with L. knudseni,

L. myersi, and L. pentadactylus. Leptodactylus paraensis is

smaller (male SVL 99–129 mm, female SVL 110–140 mm)

than L. knudseni (male SVL 94–170 mm, female SVL 102–

154 mm). The dorsolateral folds in L. paraensis are inter-

rupted; most L. knudseni have continuous dorsolateral

folds. Juvenile L. paraensis lack green coloration in life;

juvenile L. knudseni are often green on the dorsum in life.

Sexually active males of L. paraensis have a pair of black

chest spines; sexually active L. myersi males lack chest

spines. Leptodactylus myersi typically occurs on rocky

outcrops; L. paraensis does not occur on rocky outcrops;

the species have allopatric distributions. Leptodactylus

paraensis dorsolateral folds are interrupted and extend

no further from the eye to the sacrum; the dorsolateral

folds of L. pentadactylus are either continuous or, if inter-

rupted, extend beyond the sacrum.



Distribution. Rainforest habitats in eastern Amazonia in

the Brazilian states of Mato Grosso and Pará (Fig. 75).

Leptodactylus pentadactylus (Laurenti, 1768)

(Plate 7A)

Rana pentadactyla Laurenti, 1768:32. Type locality: “In-

diis;” corrected to Surinam by Müller, 1927:276.

Type(s): By indication including frog illustrated

by Seba, 1734: pl. 75, fig. 1 and Laurenti’s “Var. )

specimen[s] in “Museo Illustrissini Comitis Turri-

ani” [current location unknown and presumed lost].

Neotype locality: “Suriname, Marowijne, Lelyge-

bergte, Suralcokamp.” Neotype: RMNH 29559, adult

male, designated by Heyer, 2005:310).

Rana gigas Spix, 1824:25. Type locality: “in locis paludosis

fluminis Amazonum,” Brazil. Types: Not specifically

stated but including animal figured on plate 1 of

the original publication; ZSM 89/1921 (now lost)

according to Hoogmoed and Gruber, 1983:355 and

Glaw and Franzen, 2006:175. Synonymy by Pe-

ters, 1872:198, 225; Boulenger, 1882:241; Heyer,

1979:26. Preoccupied by Rana gigas Wallbaum, 1784

(= Bufo marinus); see Smith et al., 1977.

Figure 75. Distribution map of Leptodactylus paraensis.




S55


Rana coriacea Spix, 1824:29. Type locality: “aquis lacus-

tribus fluvii Amazonum” = Amazon River, Brazil.

Holotype: Not specifically designated, but includ-

ing animal figured on plate 5, figure 2 of the origi-

nal publication; ZSM 2502/0 [now lost] according

to Hoogmoed and Gruber, 1983:355 and Glaw and

Franzen, 2006:175. Synonymy by Peters, 1872:205,

225; Heyer, 1979:26.

Rana pachypus bilineata Mayer, 1835:24. Type locality: Not

stated. Type(s): Deposition not stated, presumed

lost. Named as a synonym of Rana gigas Spix, 1824.

Not addressed by Heyer, 2005:320, 322.

Doryphoros gigas: Mayer, 1835:28, plate III, fig. 8.

Gnathophysa gigas: Cope, 1866:73.

Cystignathus pentadactylus: Peters, 1872:198.

Leptodactylus pentadactylus: Boulenger, 1882:241.

Leptodactylus goliath Jiménez de la Espada, 1875:57. Type

localities: “Archidona [Oriente del Ecuador] … and

Chinitambo, Sierra de Guacamayos [Or. Del Ecau-

dor]; locality of lectotype given in error as “Quijos,

Ecuador” by Heyer and Peters, 1971:167 according

to González-Fernández, García-Díez, and San Se-

gundo, 2009:273, who noted that the lectotype is

from “Archidona [Oriente de Ecuador].” Syntypes:

MNCN (3 specimens); MNCN 328 designated lecto-

type by Heyer and Peters, 1971:167. Synonymy by

Boulenger, 1882:242; Heyer and Peters, 1971:167;

Heyer, 1979:26.

Leptodactylus pentadactylus – Nieden, 1923:472.

Leptodactylus macroblepharus Miranda-Ribeiro, 1926:144.

Type locality: “Manáos–Amazonas”, Brazil. Lecto-

type: MZUSP 377, adult male. Synonymy by Heyer,

1974b:43.

Leptodactylus pentadactylus pentadactylus: Müller,

1927:276.

Leptodactylus (Pachypus) pentadactylus: Lutz, 1930:1,21.

Leptodactylus pentadactylus dengleri Melin, 1941:51. Type

locality: “Roque, [San Martín,] Perú,” noted by Hey-

er, 2005:322 to be at 06°24’S, 76°48’W. Type: GNM

497 designated lectotype by Heyer, 2005:322. Syn-

onymy by Heyer, 1979:26.

Leptodactylus pentadactylus rubidoides Andersson,

1946 “1945”:51. Type locality: “Rio Pastaza,” eastern

Ecuador. Holotype: NRM 1928, juvenile female. Syn-

onymy by Heyer and Peters, 1971:168; Heyer, 1979:26.

Etymology. From the Greek penta (five) and dactylos (fin-

ger, toe). Seba’s illustrator for Rana pentadactyla obviously

took liberties with the specimen being illustrated. The il-

lustration (Seba, 1734: plate 75, figure 1) unambiguously

shows five fingers. No known frogs have five fingers.


174.2 mm (X = 153.2 mm), male SVL 100.2–195.0 mm

(X = 140.3 mm); adult male snout not spatulate; male

thumb usually with one tiny to small spine, male thumb

often lacking spines, male thumb rarely with one moder-

ate spine; males lacking chest spines; light upper lip stripe

absent; dorsal folds absent; dorsolateral folds usually

complete from eye to groin, complete from eye to sacrum,

or interrupted between sacrum and groin; lateral folds ab-

sent; posterior thigh lacking a light stripe; upper shank

barred; belly usually dark with small light vermiculations,

or often with large light vermiculations, or rarely mottled

or uniform dark; toes lacking flexible lateral fringes, toes

may have non-flexible ridges (Heyer, 2005:322–324).

Similar species. Leptodactylus pentadactylus has an

Amazonian distribution that overlaps with L. knudseni,

L. labyrinthicus, L. myersi, L. paraensis and L. stenodema.

Leptodactylus pentadactylus occurs in the tropical wet for-

ests; L. labyrinthicus occurs in open formations (the forest

canopy is not closed) within Amazonia, L. myersi is lim-

ited to rocky outcrops, L. knudseni occurs in primary rain

forest, secondary forest, and open habitats, the few data

for L. paraensis indicate that it is also limited to primary

rain forest habitat. Most L. pentadactylus have a pair of

well-developed and continuous dorsolateral folds from

the eye to at least the sacrum; most L. labyrinthicus and

L. paraensis have less developed and usually incomplete

folds. Sexually active male L. pentadactylus usually lack

a large black spine on each thumb; sexually active male

L. knudseni, L. labyrinthicus, L. myersi, and L. paraensis

have a large black spine on each thumb. Sexually active

male L. pentadactylus lack chest spines; sexually active

L. knudseni, L. labyrinthicus, and L. paraensis have a pair of

black chest spines. The dorsolateral fold originates from

the posterior eye in L. pentadactylus; the dorsolateral fold

originates from above the posterior edge of the tympa-

num in L. stenodema.


92 mm; oral disk terminal; tooth row formula 1/2(1);

dorsal part of caudal musculature light brown, fins pale

cream (Menin et al., 2010). Hero (1990) illustrated and

briefly described larvae at stage 39; description and illus-

tration of larvae at stage 30 and their oophagous habit

was recently reported (Heyer et al., 2011).

Advertisement call. Mean dominant (= fundamental)

frequency among individual ca. 680–1,030 Hz; call du-

ration 0.18–0.40 s; calls pulsed, 12–18 pulses/call; call

frequency modulated, a rising whoop at least in first half

of call; call = note rate 4–37 calls/min; no clear harmonic

structure (Heyer, 2005:324) (Fig. 76).

Distribution. Leptodactylus pentadactylus occurs in closed

canopied rain forest habitat throughout the Amazonian

Morphoclimatic Domain as defined by Ab’Sáber (1977)

(Fig. 77).




S56


Leptodactylus peritoaktites Heyer, 2005 (Plate 7B)

Leptodactylus peritoaktites Heyer, 2005:325. Type local-

ity: “Hacienda Equinox, 38 km NNW of Santo Do-

mingo de los Colorados, Esmeraldas, Ecuador, 1000’,

00°03’S, 79°20’W.” Holotype: USNM 196739, adult

male.

Etymology. From the Greek peritos (west) and aktites

(coast dweller), in allusion to the geographic distribution

of the species.


(n = 5), male SVL 124.0–146.3 mm (n = 3); adult male

snout not spatulate; males usually with a moderate to

large thumb spine; males lacking chest spines; upper

light lip stripe absent (upper lip usually with dark trian-

gular marks); dorsal folds absent; dorsolateral folds usu-

ally complete from at least ¼ to full distance from eye to

sacrum or complete to at least between sacrum and some

distance to groin; lateral folds interrupted or absent; belly

usually dark with large light discrete spots or often mot-

tled, uniformly dark, or dark with small light vermicula-

tions; sides of toes weakly ridged (not fringed) (Heyer,

2005:325–327).

Similar species. In comparing L. peritoaktites with other

species, it is important to note that in the original de-

scription (Heyer, 2005) the male secondary characteris-

tics section on pages 284–285 includes errors in the text

with respect to specimens from geographic areas F and G

(p. 283, figure 7). The text on p. 326 for L. peritoaktites

is correct for adult males: male thumb usually with one

moderate to large spine; male thumb often lacking spines;

males without chest spines. The text on p. 329 for L. rho-

domerus is correct for adult males: male thumb with one

tiny to small spine; males without chest spines.

Leptodactylus peritoaktites occurs on the coastal low-

lands of Ecuador. The only other species of Leptodactylus

that occur in the coastal lowlands of Ecuador that lack toe

fringes are L. labrosus, L. rhodomerus, and L. ventrimacu-

latus. In life, juvenile L. peritoaktites have bright red col-

oration on the posterior thighs and groin (adult life col-

oration not known); juvenile (and adult) L. labrosus and

L. ventrimaculatus lack red coloration on their posterior

thighs. Sexually active male L. peritoaktites have a single

moderate to large black spine on each thumb and never

exhibit the vermiculated belly pattern of L. rhodomerus;

sexually active L. rhodomerus males have one tiny to

small white or black spine on the thumb and a dark belly

with large light vermiculations. The outer tarsal surface

of L. peritoaktites is smooth; the outer tarsal surfaces of

L. rhodomerus and L. ventrimaculatus have white tubercles;

the outer tarsal surfaces of L. labrosus usually have scat-

tered white tubercles (78% of specimens). Adult Lepto-

dactylus peritoaktites are larger (female SVL 115–133 mm,

male SVL 124–146 mm) than L. labrosus (female SVL 50–

71 mm, male SVL 48–67 mm).

Figure 76. Advertisement call of Leptodactylus pentadactylus (recording

USNM 251).

Figure 77. Distribution map of Leptodactylus pentadactylus.

Figure 78. Advertisement call of Leptodactylus peritoaktites (recording

USNM 98).




S57



Advertisement call. Dominant frequency ca. 860 Hz (re-

cording too poor to determine accurately); call duration

0.2–0.3 s; each call with 5–8 pulses; rising frequency mod-

ulations throughout call; call rate 34–37/min; no clear

harmonic structure (Heyer, 2005:327) (Fig. 78).

Distribution. Coastal Ecuador (Fig. 79).

Leptodactylus rhodomerus Heyer, 2005 (Plate 7C)

Leptodactylus rhodomerus Heyer, 2005:327. Type local-

ity: “campamento Chancos, Vereda Campo Alegre,

Municipio de Restrepo, Valle de Cauca, Colombia,

460 m, 03°58’N, 76°44’W.” Holotype: ICNMHN

13322, adult male.

Etymology. From the Greek rhodon, rose, and meros,

thigh, in reference to the red coloration on the posterior

thighs in life.

Adult morphology. Large, female SVL 133.5–157.8 mm,

male SVL 112.2–143.8 mm; adult male snout not spatu-

late; male thumb with one tiny to small black spine; males

without chest spines; light upper lip stripe absent; dor-

sal folds absent; dorsolateral folds usually complete from

eye to groin; lateral folds interrupted or absent; poste-

rior thigh without a light stripe; upper shank barred;

belly usually dark with light vermiculations or spots; toes

ridged (not fringed) (Heyer, 2005:327–330).

Similar species. Leptodactylus rhodomerus is most similar

morphologically to L. pentadactylus and L. peritoaktites,

which have allopatric or parapatric distributions with

L. rhodomerus. Leptodactylus rhodomerus occurs in the wet

tropical forest regions of western Colombia and adjacent

Ecuador; L. pentadactylus occurs in the Amazonian wet

tropical forests. Leptodactylus rhodomerus has bright red

markings on the posterior thigh surfaces in life; L. penta-

dactylus does not have red on the thighs in life. Leptodac-

tylus rhodomerus has a parapatric distribution with L. sav-

agei to the north and L. peritoaktites to the south along

Pacific coastal South America. Sexually active male L. rho-

domerus have single tiny white to small white or black

thumb spines and lack chest spines; sexually active male

L. savagei have a single large black spine on each thumb

and have a pair of black chest spines. Leptodactylus rhodo-

merus specimens often have extensive distinct light areas

(bright red in life) on the posterior thigh surfaces; L. sav-

agei individuals rarely have this pattern. Sexually active

L. rhodomerus males have one tiny to small spine on the

thumb and a dark belly with large light vermiculations;

sexually active male L. peritoaktites have a single moderate

to large thumb spine and never exhibit the vermiculated

belly pattern of L. rhodomerus. Leptodactylus rhodomerus

commonly have continuous to interrupted large flank

folds.



Distribution. Chocó region of Pacific coastal Colombia

and northern coastal Ecuador (Fig. 80).

Figure 80 Distribution map of Leptodactylus rhodomerus.

Figure 79. Distribution map of Leptodactylus peritoaktites.




S58


Leptodactylus rhodomystax Boulenger, 1884 “1883”

(Plate 7D-E)

Leptodactylus rhodomystax Boulenger, 1884 “1883”:637.

Type locality: “Yurimaguas, Huallaga River, [Loreto,]

Northern Perú.” Syntypes: BMNH (2 specimens);

BMNH 1947.12.17.81 designated lectotype by Hey-

er, 1979:30, juvenile.

Leptodactylus stictigularis Noble, 1923:293. Type locality:

“Kartabo, British Guiana.” Holotype: AMNH 10398,

adult male. Synonymy by Parker, 1935:508; Heyer

1979:30.

Etymology. From the Greek rhodon, rose and mystax, up-

per lip.


91.4 mm (X = 78.6 mm), male SVL 59.0–89.6 mm


males with one black thumb spine and a pair of black

chest spines; upper lip with a distinct light stripe; dor-

sal folds absent; a pair of distinct, complete dorsolateral

folds; lateral folds interrupted or absent; posterior thigh

with distinct light spots on a dark background, no light

thigh stripe; upper shank barred or uniform brown or

gray; belly gray with large irregular spots at least ante-

riorly; toes with weak lateral ridges or smooth (Heyer,

1979:30–31).

Similar species. Leptodactylus rhodomystax occurs in am-

azonian Bolivia, Brazil, Colombia, Ecuador, French Gui-

ana, Perú, and Suriname. Other species that occur with

L. rhodomystax that share lack of toe fringes and have

complete dorsolateral folds in some or all individuals are

L. didymus, L. elenae, L. fuscus, L. knudseni, L. mystaceus,

L. paraensis, L. pentadactylus, L. rhodonotus, and L. steno-

dema. All these species lack the characteristic posterior

thigh pattern of distinct light spots on a dark background

of L. rhodomystax. Leptodactylus rhodomystax lacks a light

longitudinal stripe on the posterior thigh; L. didymus,

L. elenae, L. fuscus, and L. mystaceus have light posterior

thigh stripes. Leptodactylus rhodomystax has a distinct

light upper lip stripe (brilliant white or reddish in life);

L. knudseni, L. paraensis, L. pentadactylus, and L. stenode-

ma lack light upper lip stripes.



2(2)/3; tail black or dark brown (Rodrigues et al., 2007).

Advertisement call. Dominant frequency (= fundamen-

tal frequency 3,700–5,400 Hz; call duration 0.12–0.23 s;

call a single pulse; rising frequency modulations for most

of call; call rate 0.23/s; calls with harmonic structure

(Zimmerman and Bogart 1988:104–105) (Fig. 81).

Distribution. Amazonian Basin and Guyana Shield

(Fig. 82).

Leptodactylus rhodonotus (Günther, 1869)

(Plate 7F)

Cystignathus rhodonotus Günther, 1869 “1868”:481. Type

locality: “Chyavetes [= Chayavitas], Eastern Perú.”

Holotype: BMNH 1947.2.17.39, sex unknown, pre-

sumably juvenile.

Gnathophysa rubido Cope, 1874:128. Type locality: “Moya-

bamba, [San Martín,] Perú.” Syntypes: Total of 3

specimens, ANSP 11392 (female), ANSP 11394

(male) and MCZ 4780 (ANSP 11393, male, exchanged

to ANSP; Barbour and Loveridge, 1929:293); MCZ

4780 designated lectotype by Heyer, 1969c:3. Syn-

onymy by Heyer, 1969c:3.

Leptodactylus rubido: Boulenger, 1882:243.

Leptodactylus rhodonotus: Boulenger, 1882:239.

Figure 81. Advertisement of Leptodactylus rhodomystax (recording

USNM 255).

Figure 82. Distribution map of Leptodactylus rhodomystax.




S59


Pleurodema (Gnathophysa) rubida: Knauer, 1883:106. Er-

ror for rubido. Leptodactylus rubidus – Boulenger,

1884 “1883”:637. Error for rubido.

Etymology. From the Greek rhodon, rose, red and nōtos,

back.


89.7 mm (X = 74.2 mm), male SVL 54.4–79.4 mm

(X = 66.9 mm); male snout not spatulate; males with a

pair of black spines on thumb; all males larger than

65 mm SVL with a pair of black chest spines; light upper

lip stripe rare, most individuals with uniform or dark tri-

angles on upper lip; dorsal folds absent; a pair of dorso-

lateral folds extending from eye to sacrum or groin; lat-

eral folds interrupted or absent; posterior thigh without

a light longitudinal stripe; upper shank with transverse

bars or uniform; belly dark with various kinds of light

marks; juveniles with pronounced lateral ridges on toes

(not fringed), adults lacking lateral toe ridges and fringes

(Duellman, 2005:289; Heyer, 1979:30–32).

Similar species. Leptodactylus rhodonotus occurs on the

western slopes of the Andes in Bolivia and Perú. Other

species that occur with L. rhodonotus and have a pair of

dorsolateral folds extending from eye to sacrum or groin

and lacking a light stripe on the posterior thigh in at least

some specimens that occur with L. rhodonotus are: L. knud-

seni, L. leptodactyloides, L. pentadactylus, L. petersii, L. podi-

cipinus, L. rhodomystax, L. stenodema, and L. wagneri. The

toes of adult L. rhodonotus are neither fringed nor ridged

whereas toes of juveniles have pronounced lateral ridges;

toes are fringed in juvenile and adult L. leptodactyloides,

L. petersii, L. podicipinus, and L. wagneri. Leptodactylus rho-

donotus is a moderate size species (adults 54–90 mm SVL)

with two spines per thumb in adult males; L. knudseni and

L. pentadactylus are large species (adult SVL 94–195 mm)

and adult males have a single spine on each thumb. The

posterior thigh of L. rhodonotus is variably mottled; L. rho-

domystax has a thigh pattern of distinct light spots on a

dark background. The dorsolateral folds of L. rhodonotus

originate at the eye; the dorsolateral folds in L. stenodema

originate at the level of the posterior tympanum.



la 2(2)/3[1]; tail mottled (Duellman, 2005:290; Heyer

1969c:3–4).


quency 1,680–2,530 Hz; call duration 0.045–0.066 s; call

pulsatile; rising frequency modulation most notable in

first half of call; call rate 106–214/min; harmonic struc-

ture present (Duellman, 2005:290; Köhler and Lötters,

1999:217–218) (Fig. 83).

Distribution. Western slopes and adjacent lowlands of

Bolivia and Peru (Fig. 84).

Leptodactylus rugosus Noble, 1923 (Plate 8A)

Leptodactylus rugosus Noble, 1923:297. Type locality:

“near Kaieteur Falls, British Guiana [= Guyana].”

Holotype: AMNH 1169, adult male.

Etymology. From the Latin rugosus, wrinkled.


73.5 mm (X = 61.0 mm), male SVL 50.9–71.6 mm

(X = 58.9 mm); adult male snout not spatulate; adult males

with one or two black thumb spines; adult males with a

pair of black chest spines; chin/throat tubercles absent;

upper lip without a light stripe; dorsal folds absent; dorso-

lateral folds short or absent; lateral folds absent; posterior

thigh without light stripe; upper shank barred, spotted, or

Figure 83. Advertisement of Leptodactylus rhodonotus (recording USNM

305).

Figure 84. Distribution map of Leptodactylus rhodonotus.




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blotched; belly dark with various kinds of light marks to

almost uniformly light with very few melanophores; toes

ridged or smooth, not fringed (Duellman, 1997:25–26;

Heyer, 1979:32–35; Heyer and Thompson, 2000:1–5).

Similar species. Leptodactylus rugosus occurs on rocky

habitats in Venezuela and Guyana. The only other

similar species occurring on rocky outcrop habitats is

L. lithonaetes, which occurs only in Colombia and Venezu-

ela (apparently the two species have allopatric distribu-

tions). The sole morphological features that differentiate

L. lithonaetes from L. rugosus are secondary male charac-

ters. Leptodactylus rugosus males have one or two thumb

spines and all adult male L. rugosus lack chin tubercles;

L. lithonaetes adult males have a single thumb spine and

have a patch of brown/black tubercles on the chin/throat.


36.1 mm; oral disk ventral; tooth row formula 2(2)3[1];

tail mottled (Heyer, 1995:709, 711).


cy 600–2,700 Hz (Heyer 1979:34) or 1,670–2,540 Hz

(Duellman, 1997:26); call duration 0.52–0.67 s; calls

with numerous pulses; rising frequency modulations

much more pronounced in first half of call; call rate ca. 3/

min; harmonic structure present or absent (Duellman,

1997:26; Heyer, 1979:34–35; Heyer and Barrio-Amorós,

2009:285–287) (Fig. 85).

Distribution. Rocky outcrops in Venezuela and Guyana

(Fig. 86).

Leptodactylus savagei Heyer, 2005 (Plate 8B)

Leptodactylus savagei Heyer, 2005:330. Type locality:

“Rincon de Osa, Puntarenas, Costa Rica, 08°42’N,

83°29’W.” Holotype: USNM 227652, adult male.

Etymology. “The species is named in honor of Jay M.

Savage for his substantial contributions to furthering bio-

logical research in the Neotropics in general and those of

the Middle American herpetofauna in particular.”


164.1 mm (X = 137.1 mm), male SVL 106.0–156.3 mm


males with a single tiny to large black thumb spine; breed-

ing males with a pair of chest spines; light upper lip stripe

absent; dorsal folds absent; dorsolateral folds may be

continuous from eye to ¼ distance to sacrum, continuous

from eye to groin, or intermediate lengths in between;

lateral folds interrupted or absent; posterior thigh usu-

ally dark with varying light marks, rarely distinctly light

with few irregular dark marks; upper shank barred; belly

dark with various kinds of light marks; toes ridged or

smooth, not fringed (Heyer, 2005:330–333; Heyer et al.,

2010b:1–19).

Similar species. Leptodactylus savagei occurs from Hon-

duras to north coastal Colombia. Within this distribution,

L. savagei differs from L. insularum, L. melanonotus, and

L. silvanimbus by lacking toe fringes and from L. fragilis,

L. fuscus, and L. poecilochilus by lacking a longitudinal light

stripe on the posterior thigh. Leptodactylus savagei and

L. rhodomerus apparently have a parapatric distribution

pattern, with L. savagei occurring in north coastal Colom-

bia and L. rhodomerus occurring in the Colombian Choco

and adjacent Pacific coastal rainforests in neighboring Ec-

uador. Sexually active L. savagei males have a single large

black thumb spine and a pair of black chest spines, and

the posterior thigh patterns of L. savagei specimens are

usually dark with varying light marks, rarely distinctly

light with few irregular dark marks; sexually active male

L. rhodomerus have a tiny white to small white or black

spine on each thumb and no chest spines, while the pos-

terior thigh pattern of L. rhodomerus individuals is often

distinct with extensively light areas (bright red in life)

with a few irregular dark markings.

Figure 85. Advertisement of Leptodactylus rugosus (recording USNM

113).

Figure 86. Distribution map of Leptodactylus rugosus.




S61



83 mm; oral disk terminal; tooth row formula 2(2)/3(1);

tail mottled (Heyer, 1970b “1968”:181, 195, fig. 9, 197,

fig. 14, 199, fig. 19).


cy 300–520 Hz; call duration 0.24–0.42 s; calls (= notes)

with 5–13 pulses/call; rising frequency modulations

throughout call; call rate 40–49 calls (= notes)/s; calls with

harmonic structure (Heyer et al., 2010b:2) (Fig. 87).

Distribution. Honduras through Panamá and north

coastal Colombia (Fig. 88).

Leptodactylus stenodema Jiménez de la Espada,

1875 (Plate 8C)

Leptodactylus stenodema Jiménez de la Espada, 1875:64.

Type locality: “San José de Moti [Canton de Quíjos].”

Napo, Ecuador. (Confirmed by González-Fernández

et al., 2009:273). Syntype: MNCN (2 specimens);

MNCN 190 designated lectotype by Heyer and

Peters, 1971:168, adult female, now numbered

MNCN 1687 according to González-Fernández

et al., 2009:273.

Leptodactylus vilarsi Melin, 1941:52. Type locality: “Tar-

acuá, Rio Uaupés, [Amazonas,] Brazil”. Holotype:

GNM 498, adult female. Synonymy by Heyer,

1979:14.

Etymology. From the Greek stenos (narrow) and demas

(body).


66.0–105.0 mm (X = 90.2 mm) mm, male SVL 75.6–

99.7 mm (X = 86.0 mm); adult male snout not spatulate;

males without thumb spines or chest spines; light upper

lip stripe absent; dorsal folds absent; distinct dorsolateral

folds; lateral folds absent; no light stripe on posterior thigh;

upper shank with wide or narrow bars; belly dark with var-

ious kinds of light marks; lateral surface of toes smooth or

weakly ridged (not fringed) (Heyer, 1979:34–36).

Figure 87. Advertisement of Leptodactylus savagei.

Figure 88. Distribution map of Leptodactylus savagei.

Figure 89. Advertisement of Leptodactylus stenodema.

Figure 90. Distribution map of Leptodactylus stenodema.




S62


Similar species. Leptodactylus stenodema is the only spe-

cies in the genus in which the dorsolateral fold originates

just posterior to the tympanum rather than the eye (other

species with dorsolateral folds with posterior eye and dor-

solateral fold abutting).



cy 120–680 to 760–900 Hz; call duration 0.26–0.36 s; call

a single multi-pulsed note; modest rising frequency mod-

ulations throughout call; call rate 30/min; no harmonic

structure (Heyer, 1979:36; Lescure and Marty, 2000:348,

374) (Fig. 89).

Distribution. Lowland Amazonian rainforests (excluding

Bolivia) of Brazil, Colombia, Ecuador, Peru, French Gui-

ana, and Surinam (Fig. 90).

Leptodactylus turimiquensis Heyer, 2005 (Plate 8D)

Leptodactylus turimiquensis Heyer, 2005:333. Type locali-

ty: “Caripito, Monagas, Venezuela, ~ 100 m, 10°08’N,

63°06’W.” Holotype: AMNH 70667, adult male.

Etymology. Jaime E. Péfaur, at W.R. Heyer’s request,

kindly suggested naming this species L. turimiquensis af-

ter the Serranía de Turimiquire, which encompasses the

known distribution of the species. Spanish and English

authors have transliterated the indigenous name for the

mountain range involved as Turimiquire and Turumiquire.

Adult morphology. Large, female SVL 122.4–128.0 mm,

male SVL 127.2–160.0 (X = 144.0 mm); adult male snout

not spatulate; adult males with a single black thumb spine

and often with a prepollical bump; breeding males with a

pair of black chest spines; light upper lip stripe absent; dor-

sal folds absent; dorsolateral folds often absent, rarely con-

tinuous from eye to groin; lateral fold interrupted; poste-

rior thigh without a light stripe; upper shank barred; belly

dark with various light marks (Heyer, 2005:317, 333–335).

Similar species. Leptodactylus turimiquensis is the only

large species of Leptodactylus without fringed toes that

occurs in the Serranía de Turimiquire, Venezuela.


Advertisement call. Dominant frequency about 400 Hz;

call duration 0.33 s; call of a single note of about 9 pulses;

call weakly frequency modulated; (call rate not given);

well defined harmonics (Rivero and Eloy Esteves, 1969:3

published an audiospectrogram but provided not de-

scriptive data; herein data are interpreted from their

audiospectrogram).

Distribution. Serranía de Turimiquire, Venezuela (Fig. 91).

Leptodactylus vastus Lutz, 1930 (Plate 8E-F)

Leptodactylus vastus Lutz, 1930:32. Type locality: “Inde-

pendencia [Parayba],” Brazil, now Guarabira, Paraí-

ba, at 06°51’S, 35°29’W. Lectotype: AL-MN 70, adult

male. See Comments, below.

Etymology. From the Latin vastus (enormous), charac-

terizing the large size of the species.


167.0 mm (X = 150.7 mm), male SVL 135.0–180.3 mm


males usually with one large thumb spine, rarely with a

tiny or small spine; breeding males with a pair of chest

spines; no light stripe on upper lip; dorsal folds absent;

dorsolateral folds usually interrupted from ½ to full dis-

tance from eye to sacrum, rarely continuous from at least

¼ to full distance from eye to sacrum, rarely interrupted

to at least between sacrum and some distance to groin;

lateral fold interrupted or absent; posterior thigh without

a light stripe; upper shank barred; belly usually labyrin-

thine patterned, often mottled or uniform dark, or light

with dark vermiculations, or dark with light vermicula-

tions; lateral surfaces of toes ridged (not fringed) (Heyer,

2005:297, 335–337, 347–348).

Similar species. Leptodactylus vastus occurs in open for-

mations in the Brazilian states of Alagoas, Ceará, Goiás,

Maranhão, Pernambuco, Rio Grande do Norte, and Ser-

gipe. The only similar species of large size, toes not fringed,

and no light posterior thigh stripe is L. labyrinthicus. The

available distributional data are inadequate to ascertain

whether L. labyrinthicus has a parapatric distribution

Figure 91. Distribution map of Leptodactylus turimiquensis.




S63


with L. vastus or whether there is some geographic over-

lap of the two species. There are no definitive morpho-

logical features that consistently separate L. vastus from

L. labyrinthicus. Adolfo Lutz (1926a) published two color

plates (30, 31) containing dorsal and ventral figures of the

species he subsequently named as L. vastus. Plate 30, fig-

ures 3 and 4 have yellow mottling on the venter and pos-

terior thigh surfaces. Plate 31, figures 1 and 2 have white

mottling on the venter and posterior thighs; presumably

the specimen illustrated was faded at the time it was illus-

trated. Lutz (1926a:143) considered L. labyrinthicus a syn-

onym of L. pentadactylus. His color plate 30, figures 1–2,

shows bold red mottling on the posterior thighs and a

labyrinthine ventral surface of brown and yellow. Further

fieldwork is needed to verify if the color differences be-

tween Lutz’s figures are diagnostic for L. labyrinthicus and

L. vastus. The two species differ in their advertisement

calls. Leptodactylus vastus has a pulsed advertisement call;

L. labyrinthicus has an unpulsed advertisement call Heyer

et al. (2005) provided genetic data that supported L. laby-

rinthicus, L. paraensis, and L. vastus as valid species.


38–40) 52 mm; oral disk anterior; tooth row formulae

1/2-3(1); tail mottled (Vieira et al., 2007:62–63).


quency ca. 430 Hz; call duration 0.14–0.19 s; call of single

pulsed note; rising frequency modulations throughout

call; call rate 54–61/min; call with harmonic structure

(Heyer, 2005:296–297, 336) (Fig. 92).

Distribution. Open habitats in northeast Brazil (Fig. 93).

Comments. Adolpho Lutz proposed the name Lepto-

dactylus vastus for three specimens that he had previ-

ously reported and figured as L. ? gigas. When the Lutz

collection was transferred from the Instituto Oswaldo

Cruz to MNRJ, there was but a single specimen labeled

as the type of L. vastus, AL-MN 70 (Ulisses Caramaschi,

pers. comm.). Bokermann (1966:75) listed in his type lo-

cality publication “Leptodactylus vastus A. Lutz, 1930:4”

with the comment “Nome nôvo para Leptodactylus gi-

gas A. Lutz, 1926[a]:144.” Lutz’s English text (1930:29)

states: “The remarks made by Peters and Lorenz Mueller

on the type of Spix do not permit to refer to it the frog

from Independencia (Parahyba) mentionned [sic] in my

first paper as ? gigas. I have not been able to obtain more

specimens in the same region … I shall now call this spe-

cies Leptodactylus vastus n. sp.” Bokermann’s characteriza-

tion of Lutz applying a new name for Leptodactylus gigas is

misleading. Lutz (1926a) may have thought that the three

specimens involved were the same species as Leptodacty-

lus gigas Spix, from the Amazon river. By 1930, Lutz was

convinced that the specimens he had from the Brazilian

state of Paraíba were not conspecific with Spix’s L. gigas

from the Amazon river. Thus, Lutz 1930:29 named the

new species L. vastus for the three specimens (from Paraí-

ba) he originally thought might be conspecific with the

Amazonian L. gigas.

Leptodactylus latrans species group

Leptodactylus bolivianus Boulenger, 1898 (Plate 9A)

Leptodactylus bolivianus Boulenger, 1898:131. Type local-

ity: Bolivia, Río Madidi, Barraca. Lectotype: MSNG

28875A, male.

Leptodactylus romani Melin, 1941:54. Type locality: Brazil,

Rio Uaupés, Taracuá. Lectotype: GNM 499, juvenile.

Etymology. The species is named for the country of Bo-

livia from which the specimens were collected.

Figure 92. Advertisement call of Leptodactylus vastus (recording USNM

233).

Figure 93. Distribution map of Leptodactylus vastus.




S64



61.2–107.7 mm (X = 85.3 mm), male SVL 79.0–121.5 mm

(X = 104.6 mm); adult male snout not spatulate; sexually

active males with single large, markedly chisel-shaped

thumb spine, chin tubercles present, but no chest spines;

light upper lip stripe usually present (70% of specimens);

dorsal folds absent; dorsolateral folds well developed;

lateral folds present, interrupted or complete; posterior

thigh lacking light stripe; upper shank barred; belly uni-

form light, rarely mottled anteriorly; toes fringed (Heyer

and de Sá, 2011).

Similar species. The species that co-occur with Lepto-

dactylus bolivianus in the Amazonian portions of Bolivia,

Brazil, Colombia, Peru, and Venezuela that have distinct

dorsolateral folds and toe fringes are L. latrans complex

species, L. petersii, and L. riveroi. Leptodactylus bolivianus

lacks dorsal folds; L. latrans complex species has dor-

sal folds. The belly is uniform light or rarely mottled in

L. bolivianus; the entire bellies of L. petersii and L. riveroi

are moderately to boldly mottled.

Larval morphology. Unknown. Available descriptions

purported to be Leptodactylus bolivianus correspond to

L. insularum (Heyer and de Sá, 2011).


quency 600–690 Hz; call duration 0.12–0.16 s; 1–2 notes/

call; rising frequencies most pronounced in first 1/3–1/2

of call; call rate 0.5/s; no apparent harmonic structure

(Heyer and de Sá, 2011) (Fig. 94).

Distribution. Central and western portions of the Ama-

zon basin in Bolivia, Brazil, Colombia, Peru, and Venezu-

ela (Fig. 95).

Leptodactylus chaquensis Cei, 1950 (Plate 9B)

Leptodactylus ocellatus var. typica Cei, 1948:308 Type lo-

cality: Not explicitly stated, presumably Tucumán,

Argentina. Anonymous, 2003:173 (Opinion 2044)

suppressed this name for purposes of synonymy.

Leptodactylus chaquensis Cei, 1950:417. Type local-

ity: Multiple localities in Argentina cited; Lavilla,

1994 “1992”:85 gave Simoca, Tucumán as the type

locality. Holotype: FML 979, adult male, specimen

lost according to Lavilla, 1994 “1992”:85.

Etymology. The name chaquensis refers to the geographi-

cal region of the Gran Chaco of Argentina.


68.1–97.6 mm (X = 76.8 mm), male SVL 65.4–94.3 mm

(X = 79.5 mm); adult male snout not spatulate; sexually

active males with a pair of keratinized thumb spines;

males without chest spines; light upper lip stripe absent;

mid-dorsal fold interrupted (Fig. 2, fold 1); a pair of com-

plete dorsal folds (Fig. 2, fold 2), a pair of complete or

interrupted auxiliary dorsal folds extending from eye to

the sacral region (Fig. 2, fold 3), dorsolateral folds (Fig. 2,

fold 4) complete from eye to groin; auxiliary lateral fold

(Fig. 2, fold 5) extending from mid-body to groin; lateral

fold (Fig. 2, fold 6) complete or interrupted; posterior

thigh almost uniform, slightly mottled, greenish in life;

upper shank barred; belly uniform light; toes with lateral

fringes (Cei, 1980:348, 350).

Similar species. Leptodactylus chaquensis from Argentina,

Bolivia, Brazil, Paraguay, and Uruguay have fringed toes

and a pair of dorsal folds. The other species sharing the

same characteristics (with potentially overlapping distri-

butions) are the L. latrans species complex and L. viridis.

Leptodactylus chaquensis almost always have complete

or interrupted auxiliary dorsal folds (Fig. 2, fold 3); no

Figure 94. Advertisement call of Leptodactylus bolivianus.

Figure 95. Distribution map of Leptodactylus bolivianus.




S65


L. latrans complex specimens have this fold. The post-tym-

panic dark stripe that extends to the forelimb may differ-

entiate southern populations (Argentina and Uruguay) of

L. chaquensis and L. latrans complex – triangular-shaped

in specimens of the L. latrans complex, not triangular in

L. chaquensis. Leptodactylus chaquensis has well-developed

dorsal folds and adult males have a pair of black spines

on each thumb; L. viridis has weak dorsal folds and adult

males have a single black spine on each thumb. Live speci-

mens of L. viridis are easily distinguished from L. chaquen-

sis and L. latrans complex specimens by their characteris-

tic overall green body coloration.

Larval morphology. Total length (Gosner 36) 42 mm;

oral disk anteroventral; tooth row formula 2/3 or 2/3[1],

P1 interruption very short when present; tail muscula-

ture uniform brown/black (data from Cei, 1980:351–352;

Heyer and Giaretta, 2009:301).

Advertisement call. Three distinctive advertisement

calls known: growls (most frequent), grunts, and trills.

Growls (Fig. 96A): dominant (= fundamental) frequency

343–515 Hz; call duration 0.41–0.66 s; call composed of

16–30 notes, notes single or double pulsed throughout

call; weak frequency modulation throughout call; call rate

46–49/s. Grunts (Fig. 96B): dominant (= fundamental)

frequency 263–343 Hz; call duration 0.10–0.12 s; call

composed of 8–10 notes/pulses per call; frequency modu-

lation not apparent; call rate 71–100/s. Trills (Fig. 96A):

Figure 96. Advertisement calls of Leptodactylus chaquensis. (A) Growl.

(B) Grunt. (C) Trill. Figure 97. Distribution map of Leptodactylus chaquensis.




S66


dominant (= fundamental) frequency 424–520 Hz; call

duration 0.48–0.81 s; call composed of 11–16 notes per

call; frequency modulation not apparent over entire call.

All three call types with at least one harmonic (Heyer and

Giaretta, 2009:295–300) (Fig. 96).

Distribution. Arid ecosystems in northern Argentina and

adjacent Bolivia, Brazil, Paraguay, and northern Uruguay;

northern extent of distribution unknown in Brazil (Fig. 97;

for new records in southern Brazil see Oda et al., 2014).

Leptodactylus guianensis Heyer and de Sá, 2011

(Plate 9C)

Leptodactylus guianensis Heyer and de Sá, 2011:35. Type

locality: “Guyana; Rupununi, Iwokrama Forest Re-

serve, Sipuruni River, Pakatau Camp, 04°45’17”N,

59°01’28”W. 85 m.” Holotype: USNM 531509, adult

male.

Etymology. Named for the species distribution that coin-

cides in large part with the Guiana Shield.


66.0–109.2 mm (X = 88.2 mm), male SVL 79.5–109.5 mm

(X = 94.2 mm); adult snout not spatulate; adult males with

a modestly chisel-shaped black thumb spine; light upper

lip stripe present or absent; dorsal folds absent; dorso-

lateral folds complete, distinct; lateral folds interrupted;

posterior thigh lacking a light stripe; upper shank barred;

belly variously mottled to no pattern (no melanophores);

toes with lateral fringes (Heyer and de Sá, 2011:35–37).

Similar species. Leptodactylus guianensis occurs in the

State of Roraima in Brazil, Guyana, Suriname, and the

State of Bolívar in Venezuela. Other species occurring in

this area with complete dorsolateral folds and toe fringes

in at least some individuals are L. latrans complex species

and L. leptodactyloides. Leptodactylus latrans complex spe-

cies have dorsal folds; L. guianensis lacks dorsal folds. The

dorsolateral folds of L. leptodactyloides are interrupted

and usually do not extend to the groin; the dorsolateral

folds of L. guianensis are complete, extending to the groin.



Distribution. Lowland portions of Guiana Shield regions

of Guyana, Suriname, Venezuela, and adjacent Brazil

(Fig. 98).

Leptodactylus insularum Barbour, 1906 (Plate 9D)

Leptodactylus insularum Barbour, 1906:228. Type local-

ity: Saboga Island in the Gulf of Panamá. Syntypes:

originally a lot of 12 specimens with the single MCZ

number 2424. The type description is not based on

a single specimen but is a composite description in-

cluding male and female data. Eleven of the 12 origi-

nal syntypes were exchanged or had new MCZ cata-

logue numbers assigned to them. A single specimen

was retained MCZ 2424. MCZ 2424 (adult female)

was designated the lectotype of L. insularum Barbour

1906 by Heyer and de Sá (2011:28).

Leptodactylus insularum: Heyer and de Sá, 2011:38–40.

Recognition of L. insularum as a distinct species.

Etymology. Name indicates original belief that the spe-

cies was restricted to islands in the Gulf of Panamá.


60.4–99.1 mm (X = 81.4 mm), male SVL 66.0–104.6 mm


with 2 round black thumb spines; light upper lip stripe in-

distinct or absent; dorsal folds absent; dorsolateral folds

well developed, complete; lateral folds distinct and com-

plete to slightly interrupted; posterior thigh without a light

stripe; upper shank barred; belly lightly to heavily mottled;

toes with lateral fringes (Heyer and de Sá, 2011:40).

Similar species. Leptodactylus insularum occurs from

Costa Rica through Panamá and along Caribbean drain-

ages of Colombia, Venezuela, and Trinidad as well as is-

lands in the Gulf of Panamá and the Colombian islands of

Providencia and San Andrés. Within its distribution, L. in-

sularum is the only Leptodactylus species with complete

dorsolateral folds and toe fringing.


35.2 mm; oral disk anteroventral; tooth row formula 2/3; Figure 98. Distribution map of Leptodactylus guianensis.




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tail musculature uniformly moderate to dark brown, tail

fins ranging from same pattern as tail musculature to

ventral tail fin with a gradient of no melanophores next

to the body to uniform brown around mid-fin (Heyer and

de Sá, 2011:24–25, 40).


cy 110–120 to 890–1,200 Hz; call duration 0.08–0.12 s;

call consisting of a single note; call frequency modulated

with rising frequencies from beginning to about 1/3 call

length; call rate 1.2–2.5/s; harmonic structure is present

or absent (Heyer and de Sá, 2011:25–27, 41) (Fig. 99).

Distribution. Costa Rica through Panamá, along Carib-

bean drainages of Colombia, Venezuela, and Trinidad, on

islands in the Gulf of Panamá, and on the Colombian is-

lands of Providencia and San Andrés (Fig. 100).

Leptodactylus latrans (Steffen, 1815) (Plate 9E)

Rana latrans Steffen, 1815:13. Neotype locality: “Vale dos

Agriões [22°25’S, 42°58’W, approx. 900 m above sea

level], Municipality of Teresópolis, State of Rio de

Janeiro, Brazil.” Neotype: MNRJ 30733, adult male,

described by Lavilla, Langone, Caramaschi, Heyer,

and de Sá, 2010:8.

Rana gibbosa Raddi, 1823:67. Type locality: Rio de Janeiro

[Brazil]. Holotype: Not stated, presumably originally

MZUF. Synonymy by Bokermann, 1965:9–12.

Rana fusca Raddi, 1823:68. Type locality: “Rio-janeiro,”

Brazil. Holotype: MZUF ???. Junior homonym of

Rana fusca Schneider. Synonymy by Bokermann,

1966:88.

Rana pygmaea Spix, 1824:30. Type locality: “Provincia Ba-

hiae,” Brazil. Type(s): Not specifically designated, al-

though including animal figured on plate 6, figure 2

of the original publication. Holotype lost from ZSM

according to Heyer, 1973:26 and Hoogmoed and Gr-

uber, 1983:356 (who implied that type material may

never have been deposited in the ZSM and noted

that RMNH 2041 might be a syntype). Synonymy by

Günther, 1859b “1858”:27; Peters, 1872:225; Bou-

lenger, 1882:247; Hoogmoed and Gruber, 1983:355.

Rana pachypus Spix, 1824:26. Type localities: “Habitat in

locis humidis Provinciae Rio de Janeiro,” [var. 1] “lo-

cis humidis Bahiae,” and [var. 2] “locis aquosis Parae,”

Brazil. See comments on types of varieties by Glaw

and Franzen, 2006:176. Syntypes: ZSM (10 speci-

mens, presumed lost), ZMB, and presumably ZMH;

ZSM 122/0.1 designated lectotype by Hoogmoed

and Gruber, 1983:356 (who implied that type mate-

rial may never have been deposited in the ZSM and

noted that RMNH 2041 might be a syntype). Syn-

onymy by Tschudi, 1838:78; Duméril and Bibron,

1841:396; Peters, 1872:225. Variety 2 shown to be

a junior synonym of Rana fusca Schneider by Peters,

1872:199 and Hoogmoed and Gruber, 1983:356.

Rana pachybrachion Wied-Neuwied, 1824:671. Type lo-

cality: “Brasiliens.” Types: Not designated. Possibly

an incorrect subsequent spelling or emendation of

Rana pachypus Spix, 1824. Synonymy by W.R. Heyer

(pers. comm. to D. Frost, Amphibian Species of the

World website accessed 27 April 2011).

Rana macrocephala Wied-Neuwied, 1825:544. Type local-

ity: “Urwälden an der Lagoa d’Arara unweit des Flus-

ses Mucuri,” Brazil (regarded as being somewhere

in southern Bahia, Brazil by Bokermann, 1966:89).

Type(s): not designated, not found at AMNH. Tenta-

tive synonymy with Leptodactylus ocellatus by Boker-

mann, 1966:89.

Cystignathus pachypus: Wagler, 1829:9; Wagler 1830:203.

Rana pachypus pachypus: Mayer, 1835:24.

Rana pachypus octolineatus Mayer, 1835:24. Type locality:

not stated. Type(s): Deposition not stated, now pre-

sumed lost.

Leptodactylus serialis Girard, 1853:421. Type locality: “Rio

de Janeiro,” Rio de Janeiro, Brazil. Syntypes: Not

Figure 99. Advertisement of Leptodactylus insularum.

Figure 100. Distribution map of Leptodactylus insularum.




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designated; USNM 7389 (2 specimens) according

to Cochran, 1961:64. Synonymy with Leptodactylus

pachypus by Jiménez de la Espada, 1875:48. Synony-

my by Girard, 1858:29; Boulenger, 1882:247.

Leptodactylus caliginosus Girard, 1853:422. Type locality:

“Rio de Janeiro, [Rio de Janeiro,] Brazil.” Syntypes:

not designated, USNM 7352 (2 specimens) accord-

ing to Cochran, 1961:64. Synonymy by Nieden,

1923:490; Lutz, 1930:22.

Leptodactylus ocellatus: Girard, 1853:420.

Cystignathus pachypus: Günther, 1859b “1858”:27.

Cystignathus caliginosus: Günther, 1859b “1858”:28.

Leptodactylus pachypus: Jiménez de la Espada, 1875:48.

Rana luctator Hudson, 1892:78. Type locality: presumably

vicinity of “Buenos Ayres,” Argentina. Holotype: lost

according to original publication. Synonymy by Gal-

lardo, 1964b:373–384; Lavilla, 1994 “1992”:87.

Rana octoplicata Werner, 1893:83. Type locality: “Norda-

merika.” Type: Not designated. Synonymy by Wer-

ner, 1894:125; Nieden, 1923:491.

Cystignathus oxycephalus Philippi, 1902:105. Type locality:

“ad Montevideo, Arrechavaleta,” Uruguay. Syntypes:

MNHNC (2 specimens) according to original publi-

cation. Synonymy by Klappenbach, 1968:150.

Cystignathus oxicephalus: Philippi, 1902:124. Incorrect

subsequent spelling.

Leptodactylus pygmaeus: Miranda-Ribeiro, 1927:15.

Leptodactylus ocellatus var. reticulata Cei, 1948:308. Type

locality: “Arroyo, Isla Apipé, Ituzaingó [Corrientes]”

and “Puerto Bemberg [Misiones],” Argentina. Syn-

types: not designated, presumably at FML.

Leptodactylus ocellatus var. bonaerensis Cei, 1949a:127.

Syntypes: Not designated, but in MACN and FML

(total of 59 examples, source of information un-

clear). Type locality: “Río Colorado y Bahía Blanca,”

Argentina. Restricted to Bahia Blanca, Argentina by

Gorham, 1966:133.

Leptodactylus latrans: Lavilla, Langone, Caramaschi, Hey-

er, and de Sá, 2010:8.

Etymology. From the Latin word latrans (barker).

Adult morphology. Large, male neotype 107.0 mm

SVL; adult male snout not spatulate; male with two

black keratinized spines on each thumb; male lacking

chest spines; light upper lip stripe absent; a pair of dor-

sal folds from the posterior interocular region to the

end of the body; a pair of complete dorsolateral folds

from the posterior corner of the eye to groin; complete

auxiliary lateral fold from the shoulder region to the

groin; complete lateral fold from the posterior corner

of the eye to groin; posterior thigh lacking light stripe;

upper shank with faint bars; belly white with scattered

irregular gray spots; toes with lateral fringes (Lavilla

et al., 2010:4–5).

Similar species. The neotype of Leptodactylus latrans can

be distinguished from L. chaquensis by the presence of an

additional pair of lesser developed but discernible dorsal

folds situated between the medial dorsal folds and the

dorsolateral folds extending from the post-tympanic re-

gion to the sacral region in most L. chaquensis.

Larval morphology. Larvae from the type locality are

unknown. Several purported descriptions corresponding

to this species complex are available; however, until the

systematics and species composition of this complex are

determined (see below), the species allocation of those

larval descriptions should be considered with caution.


Distribution. Range beyond the type locality unknown.

Comment. Leptodactylus latrans is currently considered

a species complex. In Argentina, Paraguay, and Uruguay

there are two species of the L. latrans complex that are

readily distinguishable from each other. One of them is

L. chaquensis, while the other species is a member of the

L. latrans species complex. Outside of Argentina, Para-

guay, and Uruguay the distribution of L. chaquensis is

uncertain and the taxonomic status of L. macrosternum

is unclear as to whether it is distinct from L. chaquensis.

The only solid taxonomic statement that can be made cur-

rently is that L. chaquensis from Argentina is a valid spe-

cies and L. latrans from the type locality in the State of

Rio de Janeiro, Brazil, is a valid species. The distribution

of L. latrans-like specimens outside of the type locality of

L. latrans is notoriously clouded. An analysis of color pat-

terns and size variation in the L. latrans concluded that

the data were not sufficient to determine species limits

within this complex (Heyer, 2014). For present purposes,

information provided herein for L. latrans is solely based

on the type specimen from the State of Rio de Janeiro,

Brazil.

Leptodactylus macrosternum Miranda-Ribeiro, 1926

(Plate 9F)

Leptodactylus ocellatus macrosternum Miranda-Ribeiro,

1926:147. Type locality: “Bahia”, Brazil; Boker-

mann, 1966:73, considered the type locality to be

“provàvelmente Salvador,” Bahia, Brazil. Holotype:

MZUSP 448, juvenile.

Leptodactylus ocellatus macrosternus: Miranda-Ribeiro,

1927:125. Incorrect subsequent spelling.

Leptodactylus macrosternum: Gallardo, 1964b:379. First

usage of macrosternum at the species level.

Morphology. Juvenile holotype 65 mm SVL; no informa-

tion on upper lip stripe; five longitudinal folds on each




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side of body; no information on extent of folds on each

side of body or whether folds continuous or interrupted;

no information on posterior thigh pattern, upper shank

pattern, or belly pattern; toes fringed.



Distribution. Limited to type locality.

Comment. The juvenile holotype of Leptodactylus ocella-

tus macrosternum, MZUSP 448, is in very poor condition.

Based on the holotype, it is difficult to discern what other

specimens are conspecific with it. The taxonomic status

of the holotype cannot be made until the relationships of

the L. latrans group have been clarified.

Leptodactylus silvanimbus McCranie, Wilson, and

Porras, 1980 (Plate 10A)

Leptodactylus silvanimbus McCranie, Wilson, and Porras,

1980:361. Type locality: “Belén Gualcho, Cordillera

de Celaque, Depto. Ocotepeque, Honduras, eleva-

tion 1700–1900 m [14°29’N, 88°47’W].” Holotype:

USNM 212046, adult male.

Etymology. “The scientific name silvanimbus is formed

from the Latin words silva (forest) and nimbus (rain-

cloud). The name refers to this species occurring in cloud

forests, although not restricted to that habitat.”


48.0 mm (X = 45.2 mm), male SVL 35.8–55.0 mm


males with a pair of black thumb spines; males lack chest

spines; light stripe from posterior corner of eye to tym-

panum or arm insertion present or absent; dorsal folds

absent; dorsolateral folds absent; lateral folds interrupted

or absent; no posterior thigh light stripe; upper shanks

barred to uniform; belly mottled; toes with lateral ridges

or fringes (Heyer et al., 2002).

Similar species. The only other species in Hondu-

ras with lateral toe fringing is Leptodactylus melano-

notus. Leptodactylus melanonotus and L. silvanimbus are

very similar morphologically. Leptodactylus silvanim-

bus reach larger sizes (female SVL 35.9–48.0 mm, male

SVL 35.8–55.0 mm) than L. melanonotus (female SVL

34.3–45.1 mm, male SVL 32.2–43.4 mm). Adult male

L. silvanimbus have greater arm hypertrophy than male

L. melanonotus. All L. melanonotus have toe fringes; L. sil-

vanimbus have lateral toe ridges or fringes. Leptodactylus

silvanimbus occurs at 1700–1900 m; L. melanonotus oc-

curs below 1500 m.


46.5 mm; oral disk anteroventral; tooth row formula 2(2)/3;

tail fins translucent, heavily marked with dark brown espe-

cially posteriorly, stages 30+ are considerably darker than

earlier stages (McCranie and Wilson, 2002:456–457).

Advertisement call. Dominant frequency varies from

fundamental frequencies of 420–620 Hz or first harmonic

of 1,310–1,400 Hz or third harmonic of 1,640–1,820 Hz,

or fourth harmonic of 1,380–1,920 Hz; average call du-

ration 152 ms; call of about 160 partial pulses per call;

fundamental frequency is typically initiated at 440 Hz,

quickly rising to 510 Hz, then slowly falls to 440 Hz by

end of call; call rate 22/min; harmonic structure present

(Heyer et al., 2002:743.2 (Fig. 101).

Distribution. Moderate and intermediate elevations

along the Continental Divide in the Department of Ocote-

peque in southwestern Honduras (Fig. 102).

Figure 101. Advertisement call of Leptodactylus silvanimbus (recording

USNM 113).

Figure 102. Distribution map of Leptodactylus silvanimbus.




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Leptodactylus viridis Jim and Spirandeli-Cruz, 1973

(Plate 10B)

Leptodactylus viridis Jim and Spirandeli-Cruz, 1973:13.

Type locality: “Fazenda Pedra Branca, Município de

Itajibá, Estado da Bahia,” Brazil. Holotype: MZUSP

50175, adult male).

Etymology. From the Latin viridis (green), for the overall

body coloration in life.


72.2 mm, male SVL 63.0–70.9 mm; male snout not

spatulate; males with a single black thumb spine; males

without chest spines; light lip stripe absent; very weak

dorsal folds; distinct continuous dorsolateral folds; lateral

folds interrupted or continuous; posterior thigh with-

out light stripe; upper shank barred; belly lightly speck-

led; toes with lateral fringes (Jim and Spirandeli-Cruz,

1979:707–710).

Similar species. The only other species that co-occurs

with L. viridis that has dorsal folds and toe fringing is the

Leptodactylus latrans complex species. The dorsal folds of

L. viridis are weak but discernible; the dorsal folds of the

L. latrans complex species are distinct.


Advertisement call. Unreported. The species was heard

calling on December 09–10, 2010, close to the type local-

ity (RdS pers. obs.), the area did not have rain for at least

3 days. Males were calling on muddy grounds around a

pond (not in the water) and under relatively thick vegeta-

tion. A single note call could be heard and a second longer,

but barely audible, call also was heard.

Distribution. Known from four localities in the states of

Bahia (3) and Minas Gerais (1), Brazil (Fig. 103).

Comment. The original description reports the authors’

names as “Jim, J. e Spirandelli, E.F.” Spirandeli is the cor-

rect spelling of the second author’s last name. Subse-

quently, a more complete description was published by

the authors in 1979, with Elieth Floret Spirandeli Cruz

as the second author. Presumably the second author mar-

ried and added her husband’s name (Cruz). A subsequent

citation (Freitas et al., 2001) uses the last name combina-

tion of Spirandeli-Cruz.

Leptodactylus melanonotus species group

Leptodactylus colombiensis Heyer, 1994 (Plate 10C)

Leptodactylus colombiensis Heyer, 1994:82. Type locality:

Colombia; Santander; Charalá, Virolín [= Inspección

Policía Cañaverales], confluencia del Río Cañaverales

con el Río Guillermo, vertiente occidental, 1600–

1700 m, 06°13’N, 73°05’W. Holotype: ICNMHN

7409, adult male.

Etymology. The name colombiensis refers to the geograph-

ic area of Colombia; at the time of description, Leptodac-

tylus colombiensis was known only to occur in Colombia.


62.5 mm (X = 53.3 mm), male SVL 36.0–55.9 mm


males with 2 black medium to large spines on each thumb;

males lack chest spines; distinct to indiscernible light lip

stripes from just past mid-eye or usually from posterior

corner of eye to jaw commissure; dorsolateral folds ab-

sent to complete; lateral folds absent or interrupted; light

posterior thigh stripe very distinct to indiscernible; up-

per shank barred; belly lightly to extensively mottled; toes

with lateral fringes (Heyer, 1994:82–84).

Similar species. Species occurring in the Caribbean drain-

ages of Colombia (and possibly adjacent State of Táchira in

Venezuela) with fringed toes are Leptodactylus colombiensis

and L. insularum. Dorsolateral folds, if present in L. colom-

biensis, are not bordered by dark stripes; all well-preserved

L. insularum have well developed dorsolateral folds that

are bordered by a dark stripe. Leptodactylus colombiensis

adults are smaller (female SVL less than 62 mm, male

SVL less than 56 mm) than adult L. insularum (female

SVL greater than 59 mm, male SVL greater than 66 mm). Figure 103. Distribution map of Leptodactylus viridis.




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Sexually active males of L. colombiensis lack chest spines,

L. insularum have a central patch of chest spines.

Larval morphology. Total length data not reported. Oral

disk anteroventral; tooth row formula 2/3; tail fins uni-

formly dark (data from illustration in Lynch, 2006:453).


cy of initial pulse of 620–740 Hz, remainder composed of

5–8 partial pulses modulating between 1,470–1,980 Hz;

call duration 0.031–0.034 s; call rate 0.6 calls/s; no har-

monic structure (Fig. 104).

Distribution. Caribbean drainages in Colombia. The lo-

cality in the State of Táchira, Venezuela (Barrio-Amarós

and Chacón-Ortiz, 2001:55) should be verified (Fig. 105).

Leptodactylus diedrus Heyer, 1994 (Plate 10D)

Leptodactylus diedrus Heyer, 1994:86. Type locality:

Colombia; Vaupés, ½ mile NE Timbó, ~ 01°06’N,

70°01’W. Holotype: UTA 3726, adult male.

Etymology. From the Greek diedrus, sitting apart, sepa-

rated, in allusion to the distinctiveness of this species

within the Leptodactylus podicipinus-wagneri species

complex.


34.4–47.9 mm (X = 41.1 mm), male SVL 29.7–40.4 mm


two keratinized spines on each thumb, males lack chest

spines; indistinct to indiscernible light upper lip stripe;

dorsal folds absent; dorsolateral folds absent; lateral folds

absent; most (95%) individuals lack light stripes on the

posterior thighs (5% of individuals with indistinct light

stripes); upper shank barred; belly usually (80%) lack-

ing melanophores or other pattern, belly sometimes

(20%) lightly mottled; toes with lateral fringes (Heyer,

1994:86–87).

Similar species. Leptodactylus diedrus inhabits areas of

the Amazon basin and might be expected to occur with

the following Leptodactylus species with toe fringes:

L. bolivianus, L. colombiensis, L. latrans complex species,

L. leptodactyloides, L. petersii, L. podicipinus, L. riveroi,

L. validus, and L. wagneri. Leptodactylus diedrus lack dor-

solateral folds, the bellies usually lack melanophores,

the mottled ventral thigh patterns usually are in sharp

contrast to the patternless bellies, and the toe tips usu-

ally are expanded into small discs. Leptodactylus bolivi-

anus, L. latrans complex species, L. riveroi, and L. wag-

neri have distinct dorsolateral folds. The belly and thigh

patterns blend and the bellies usually have distinct pat-

terns in L. colombiensis, L. petersii, L. podicipinus, and

L. validus.


Advertisement call. Heyer (1998) described the call with

the following characteristics: dominant (= fundamental)

frequency 490–1,170 Hz; call duration 0.18–0.30 s; call

rate 0.7 calls/s; call composed of 2–6 pulses per note; call

frequency modulated, rising throughout the call; definite

harmonic structure, well developed second harmonic.

Distribution. Western Amazonia (Brazil, Colombia, Peru,

and Venezuela) (Fig. 106).

Figure 104. Advertisement call of Leptodactylus colombiensis.

Figure 105. Distribution map of Leptodactylus colombiensis.




S72


Leptodactylus discodactylus Boulenger, 1884 “1883”

(Plate 10E)

Leptodactylus discodactylus Boulenger, 1884 “1883”:637.

Type locality: Yurimaguas, Huallaga River [Loreto]

Northern Perú. Holotype: BMNH 84.2.18.44, re-

registered as BMNH 1947.2.17.40, female.

Leptodactylus nigrescens Andersson, 1946 “1945”:57. Type

locality: Rio Napo, Watershed, 400 m, Ecuador. Lec-

totype: NRM 1930, not an adult male, either juvenile

or female.

Vanzolinius discodactylus: Heyer, 1974b:88. New genus al-

location for the taxon.

Leptodactylus discodactylus: de Sá, Heyer, and Camargo,

2005:87–97 and Frost, Grant, Faivovich, Bain,

Haas, Haddad, de Sá, Channing, Wilkinson, Don-

nellan, Raxworthy, Campbell, Blotto, Moler,

Drewes, Nussbaum, Lynch, Green, and Wheeler,

2006:362 synonymized the genus Vanzolinius Hey-

er, 1974 with the genus Leptodactylus Fitzinger,

1826.

Etymology. From the Greek diskos, disk, and daktylos,

finger/toe, characterizing the species as having disk-

shaped toe tips.



male snout not spatulate; males without thumb and

chest spines; light upper lip stripe absent; no dorsal, dor-

solateral, or lateral folds; posterior thigh usually mottled,

some specimens with dark and/or light stripes; upper

shank barred; belly mottled; toes fringed (Heyer, 1970a,

1974a).

Similar species. Leptodactylus discodactylus occurs in Am-

azonian Brazil (Acre, Amazonas), Colombia, Ecuador, and

Peru. Similar species within the distribution of L. discodac-

tylus are L. bolivianus, L. diedrus, L. griseigularis, L. leptodac-

tyloides, L. pascoensis, L. petersii, L. podicipinus, and juveniles

of L. wagneri. The dorsal toe disks of L. discodactylus have

between 1–5 longitudinal grooves (visible under magnifi-

cation); all listed similar species lack dorsal longitudinal

grooves (on the dorsal toe tips) except L. diedrus. Leptodac-

tylus diedrus have a single longitudinal dorsal groove on the

largest toe disks; furthermore, the ventral and posterior

thigh patterns abut in L. diedrus, whereas the ventral and

posterior thigh patterns blend together in L. discodactylus.

Larval morphology. Duellman’s (1978) description and

Heyer’s (1998) illustration may or may not correspond

to L. discodactylus. Maximum total length (Gosner 30)

25 mm; oral disk anteroventral; tooth row formula 2/3;

tail uniform dark (Duellman, 1978:106; Heyer, 1998:5–6).

Figure 106. Distribution map of Leptodactylus diedrus.

Figure 107. Advertisement call of Leptodactylus discodactylus (recording

USNM 18).

Figure 108. Distribution map of Leptodactylus discodactylus.




S73



quency 1,160–3,190 Hz; call mean duration 0.12–0.14 s;

calls pulsed or partially pulsed (ca. 14–19 pulses/call); ris-

ing frequency throughout call, most abrupt at beginning

of call; call = note rate 1.1/s; harmonic structure weak or

absent (Heyer, 1997) (Fig. 107).

Distribution. Amazonian Brazil (Acre, Amazonas), Co-

lombia, Ecuador, and Peru (Fig. 108).

Leptodactylus griseigularis (Henle, 1981) (Plate 10F)

Adenomera griseigularis Henle, 1981:139. Type locality:

Perú, Huanuco, Potanischer Garten in Tingo Maria,

641 m. Holotype: ZFMK 31800, juvenile.

Leptodactylus griseigularis: Heyer, 1985 “1984”:97–100. First

association of griseigularis with the genus Leptodacty-

lus; L. griseigularis considered a synonym of L. wagneri.

Leptodactylus griseigularis: Heyer, 1994:87.

Etymology. From Latin griseus (gray) and gula (throat).


59.3 mm (X = 47.8) mm, male SVL 34.1–52.9 (X = 43.5)

mm; adult male snout not spatulate; adult males with a

pair of black keratinized spines on each thumb; males lack

chest spines; light posterior upper lip stripe usually indis-

tinct or absent; dorsal folds absent; dorsolateral folds of

moderate length to absent; lateral folds interrupted or

absent; posterior thigh light stripes usually indiscernible

(86%); upper shank uniform to barred; belly mottled; toes


Similar species. Leptodactylus griseigularis occurs in the

Bolivian Department of La Paz and the Peruvian Depart-

ments of Ayacucho, Huanuco, Junin, Pasco, San Martín,

and Ucayali between 100–1800 m. Other similar species

with toe fringes overlapping in distribution with L. grisei-

gularis are: L. bolivianus, L. chaquensis, L. leptodactyloides,

L. pascoensis, L. petersii, and L. podicipinus. Leptodactylus

chaquensis has a pair of dorsal folds; L. griseigularis lacks

dorsal folds. Leptodactylus griseigularis is a moderate-size

species (females 39–58 mm SVL, males 35–51 mm SVL) in

which most individuals have interrupted dorsolateral folds;

L. bolivianus is a large species (females to 88 mm SVL, males

to 94 mm SVL) in which the dorsolateral folds are complete.

Leptodactylus griseigularis is most likely to be confused with

L. leptodactyloides; the commonest posterior thigh pattern

in L. griseigularis is mottled, without any indication of light

stripes; the commonest posterior thigh pattern in L. lep-

todactyloides is with distinct light stripes; almost all male

L. griseigularis have large black thumb spines; almost all

male L. leptodactyloides have medium black thumb spines.

Leptodactylus griseigularis is smaller than L. pascoensis

(L. pascoensis females 52–67 mm SVL, males 60–61 mm

SVL). Leptodactylus griseigularis is larger than L. petersii

(L. petersii females 31–51 mm SVL, males 27–41 mm SVL);

the commonest belly pattern is a light mottle in L. griseigu-

laris, whereas the commonest belly pattern in L. petersii is

an extensive mottle in an anastomotic pattern. Leptodac-

tylus griseigularis is larger than L. podicipinus (L. podicipinus

females 30–54 mm SVL, males 24–43 mm SVL) and the

bellies of L. podicipinus often are dark with distinct small

light spots whereas the bellies of L. griseigularis are mottled.



cy 1,380–3,060 Hz; call duration 0.08–0.14 s; each call a

single pulse; calls frequency modulated, rising through

the call; call rate 1.8/s; harmonic structure equivocal

(Heyer and Morales, 1995:91–92) (Fig. 109).

Distribution. Bolivia and Perú (Fig. 110).

Figure 109. Advertisement call of Leptodactylus griseigularis.

Figure 110. Distribution map of Leptodactylus griseigularis (recording

USNM 274).




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Leptodactylus leptodactyloides (Andersson, 1945)

(Plate 11A)

Eleutherodactylus leptodactyloides Andersson,

1946 “1945”:43. Type locality: “Rio Pastaza,” eastern

Ecuador. Holotype: NRM 1945, adult male.

Leptodactylus leptodactyloides: Heyer, 1994:88.

Etymology. Andersson considered the type specimen to

be a new species in the genus Eleutherodactylus that re-

sembled frogs of the genus Leptodactylus.


56.2 mm (X = 46.3 mm), male SVL 28.3–47.9 mm


males with a pair of medium-sized black keratinized

thumb spines; males lacking chest spines; light upper

lip stripe absent between tip of snout to under eye, light

stripe from under eye to jaw commissure very distinct to

indiscernible; dorsal folds absent; dorsolateral folds ab-

sent or extending partially or totally from eye to groin;

lateral folds absent or interrupted; upper shank barred

to rarely uniform; belly mottled; toes with lateral fringes

(Heyer, 1994:88–89).

Similar species. Leptodactylus leptodactyloides occurs

sympatrically with or in the same general region as the

following Leptodactylus species with toe fringes: L. bolivi-

anus, L. colombiensis, L. diedrus, L. griseigularis, L. latrans

complex species, L. pascoensis, L. petersii, L. podicipinus,

L. riveroi, L. sabanensis, L. validus, and L. wagneri (among

these, L. leptodactyloides most closely resembles L. colom-

biensis, L. griseigularis, and L. sabanensis). Leptodactylus

leptodactyloides rarely (5% of specimens) have long dor-

solateral folds but when present they are interrupted, not

smooth; the dorsolateral folds in L. bolivianus and L. riv-

eroi are always long and complete. Leptodactylus leptodac-

tyloides is smaller than L. colombiensis (L. leptodactyloides

females 35–56 mm SVL, males 28–48 SVL; L. colombien-

sis females 40–62 mm SVL, males 36–56 mm SVL) and

fewer L. leptodactyloides (10% of specimens) have light-

spotted chins/throats than do L. colombiensis (44%).

Leptodactylus leptodactyloides almost always has some in-

dication of short to long, interrupted or continuous dor-

solateral folds; L. diedrus lacks dorsolateral folds. Almost

all L. leptodactyloides have melanophores on the belly;

most L. diedrus usually lack belly melanophores (81% of

specimens). Posterior and ventral thigh patterns blend

into each other in L. leptodactyloides; the patterns abut

in L. diedrus. The commonest posterior thigh pattern in

L. leptodactyloides is with distinct light stripes whereas in

L. griseigularis the commonest pattern is mottled, with no

indication of light stripes; almost all reproductively active

male L. leptodactyloides have a pair of medium-size black

thumb spines, almost all male L. griseigularis have a pair

of large thumb spines. Members of the L. latrans complex

have a pair of dorsal folds; L. leptodactyloides lacks dorsal

folds. Leptodactylus leptodactyloides is smaller than L. pas-

coensis (L. leptodactyloides females 35–56 mm SVL, males

28–50 mm SVL; L. pascoensis females 52–67 mm SVL,

males 60–61 mm SVL); L. leptodactyloides individuals usu-

ally have some indication of light stripes on the posterior

thigh, whereas most L. pascoensis specimens have mottled

thighs and lack light stripes. Leptodactylus leptodactyloi-

des have more intense belly patterns anteriorly and most

individuals are moderately mottled; L. petersii specimens

have more uniformly patterned bellies, often in an anas-

tomotic pattern, and most individuals have extensively

mottled bellies. Leptodactylus leptodactyloides never has

distinct light belly spots; L. podicipinus often has distinct

light belly spots. Most L. leptodactyloides have distinct

light stripes on the posterior thighs; the thighs of most

L. podicipinus are entirely mottled with no indication of

light stripes. Most L. leptodactyloides have at least indi-

cations of light posterior upper lip stripes; L. sabanensis

lacks upper lip stripes. Leptodactylus leptodactyloides dif-

fers from L. sabanensis in advertisement call. In L. lepto-

dactyloides the call duration is 0.01–0.04 s with a dominant

frequency range of 650–1,600 Hz and with maximum

energy between 1,100–1,300 Hz; in L. sabanensis the call

duration is 0.04–0.06 s with a dominant frequency range

of 900–2,300 Hz and with maximum energy between

1,400–1,800 Hz. Leptodactylus validus occurs on the Less-

er Antilles, Trinidad and Tobago, while L. leptodactyloi-

des does not. Leptodactylus leptodactyloides is larger than

mainland L. validus (L. leptodactyloides females 35–56 mm

SVL, males 28–48 mm SVL; mainland L. validus females

30–43 mm SVL, males 28–37 mm SVL). The commonest

upper lip stripe condition in L. leptodactyloides is indis-

tinct stripes with all posterior lip stripes extending from

the posterior corner of the eye; in mainland L. validus the

commonest condition is distinct stripes that often extend

from under the middle of the eye. Few L. leptodactyloides

have light spotted chin/throat patterns; many mainland

L. validus have light chin/throat spots. Leptodactylus lep-

todactyloides is smaller than L. wagneri (L. leptodactyloides

females 35–56 mm SVL, males 28–48 mm SVL; L. wagneri

females 52–82 mm SVL, males 39–61 mm SVL). Very few

L. leptodactyloides specimens have long dorsolateral folds;

most L. wagneri have long dorsolateral folds. The bellies

of L. leptodactyloides characteristically are finely mottled;

many L. wagneri have boldly mottled bellies.


28.3 mm; oral disk anteroventral; tooth row formula stag-

es 25–27 2[2]/3, stages 28–40 2/3; tail almost uniform

brown, heaviest over musculature (Heyer, 1994:89).

Advertisement call. Dominant (= fundamental) frequency

650–1,600 Hz; call duration 0.01–0.04 s; calls unpulsed




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or with 3–5 partial pulses; rising frequency modulation

throughout call; call rate 0.3–3.3 calls/s; harmonic structure

present or absent (Heyer 1994:16, 17, 37, 38, 89) (Fig. 111).

Distribution. Throughout the greater Amazon basin and

the Guianas from known elevations of 15–400 m (Fig. 112).

Leptodactylus magistris Mijares-Urrutia, 1997

Leptodactylus magistris Mijares-Urrutia, 1997:114.

Type locality: “Cerro Socopó, cerca de 30 km [por

carretera] al SO de Guajiro, Municipio Mauroa, Es-

tado Falcón, Venezuela, cerca de 1250 m.” Holotype:

EBRG 3284, adult male.

Etymology. According to Mijares-Urrutia, the Latin mag-

istris honors three of his professors: Pascual Soriano, En-

rique La Marca, and Alexis Arends.

Adult morphology. Small/moderate size, female

SVL 27.9–45.1 mm (X = 38.6 mm), male SVL 39.0–

30.1 mm; adult male snout not spatulate; males with a

pair of keratinized spines on each thumb; males lack-

ing chest spines; upper lip pattern uniform, without

stripe; dorsal folds absent; dorsolateral folds absent;

lateral folds absent; thigh with or without a light

stripe; upper shank with distinct to incomplete bars;

belly with mottling anteriorly, lacking pigment pos-

teriorly; toes with lateral fringes (Mijares-Urrutia,

1997:113–120).

Similar species. Leptodactylus magistris is known only

from the Cerro Socopó region in Venezuela. There are

no other described species having toe fringes and lack-

ing dorsolateral folds in the area where the Venezu-

elan states of Falcón, Lara, and Zulia converge. Heyer

(1994:113–114) noted that several populations in Co-

lombia and Venezuela (i.e., Lake Maracaibo, Maracaibo

Drainage, and Venezuelan Andes) could not be assigned

to diagnosable species. Further work is needed to clarify

their taxonomic status and the geographic distribution

of L. magistris.



Distribution. Cerro Socopó region in Venezuela

(Fig. 113).

Figure 113. Distribution map of Leptodactylus magistris.

Figure 111. Advertisement call of Leptodactylus leptodactyloides.

Figure 112. Distribution map of Leptodactylus leptodactyloides (record-

ing USNM 207).




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Leptodactylus melanonotus (Hallowell,

1861 “1860”) (Plate 11B)

Cystignathus melanonotus Hallowell, 1861 “1860”:485.

Type locality: “Nicaragua” restricted to “Recero, Ni-

caragua,” by Smith and Taylor, 1950:320; restriction

disputed by Dunn and Stuart, 1951:58. Holotype:

USNM 6264 according to Kellogg, 1932:88, appar-

ently lost, according to Heyer, 1970a:9; KU 84848

designated Neotype by Heyer, 1970a:11, Neotype

from “Nicaragua, Zelaya, Bonanza.”

Cystignathus echinatus Brocchi, 1877:181. Type locality:

“Rio Madre Nieja [Vieja?] [Guatemala occidental].”

Syntypes: MNHN 6322–23 according to Guibé,

1950 “1948”:30. Synonymy by Heyer, 1970a:9.

Cystignathus microtis Cope, 1879:265. Type locality: “Gua-

najuato,” Mexico (presumed to be in error by Heyer,

1970a:12). Restricted to “Apatzingán (de la Consti-

tución),” Michoacán, Mexico, by Smith and Taylor,

1950:35. Syntypes: USNM 9906, 9908, and 9909,

according to Heyer, 1970a:9 (in error). Kellogg,

1932:88 considered USNM 9906 the “type” and Co-

chran, 1961:40 considered USNM 9906 to be the

“holotype,” a lectotype designation by implication.

Synonymy by Cochran, 1961:40 and Heyer, 1970a:9.

Cystignathus perlaevis Cope, 1879:269. Type locality: “near

a well near Japana,” Oaxaca, Mexico = Tapanatepec

according to Smith and Taylor, 1948:57 = Tapana,

Tehuantepec, Oaxaca, Mexico, according to Cochran,

1961:40. Holotype: USNM 10041, female, by origi-

nal designation and according to Kellogg, 1932:89.

Synonymy by Kellogg, 1932:89; Cochran, 1961:40;

Heyer, 1970a:12.

Leptodactylus echinatus: Brocchi, 1881–1883:20.

Leptodactylus melanonotus: Brocchi, 1881–1883:20.

Leptodactylus microtis: Boulenger, 1882:244.

Leptodactylus perlaevis: Boulenger, 1882:215.

Leptodactylus occidentalis Taylor, 1937 “1936”:349. Type

locality: “Tepic, Nayarit, Mexico.” Holotype: EHT

3322 by original designation; now FMNH 100015

according to Marx, 1976:57, adult female. Synony-

my by Heyer, 1970a:9.

Etymology. From Greek mela, melan (black) and notos

(back).

Adult morphology. Small/moderate size, female SVL

34.3–48.1 mm (X = 40.6 mm), male SVL 32.2–43.4 mm


a pair of keratinized thumb spines; males lacking chest

spines; light upper lip stripe absent or light stripe from eye

to tympanum or arm; dorsal folds absent; dorsolateral folds

weak or absent; lateral folds interrupted; posterior thigh

mottled; upper shank barred; belly uniform light to mot-

tled; toes fringed (McCranie and Wilson, 2002:446–448).

Similar species. Leptodactylus melanonotus occurs from

Mexico through Panamá, extending west of the Andes in

mesic habitats of Colombia and Ecuador. The only similar

species that occur with L. melanonotus that have toe fring-

es are L. insularum and L. silvanimbus. Leptodactylus mela-

nonotus have weak or absent dorsolateral folds and adult

males have a pair of keratinized thumb spines; L. insula-

rum have well defined dorsolateral folds extending from

eye to groin and adult males have a single black spine on

each thumb. Leptodactylus silvanimbus reach larger sizes

(female SVL 35.9–48.0 mm, male SVL 35.8–55.0 mm)

than L. melanonotus (female SVL 34.3–45.1 mm, male

SVL 32.2–43.4 mm). Adult male L. silvanimbus have either

lateral toe ridges or fringes; all L. melanonotus have toe

fringes. Leptodactylus melanonotus occurs below 1500 m,

L. silvanimbus occurs at 1700–1900 m.


41.6 mm; oral disk anteroventral; tooth row formula 2[2]/3;

tail almost uniform dark (Heyer, 1970b “1968”:178–179,

figs. 8, 13, 18; McCranie and Wilson, 2002:448–449, Or-

ton, 1951:62–66, Savage, 2002:215–217).

Figure 114. Advertisement call of Leptodactylus melanonotus (recording

USNM 83).

Figure 115. Distribution map of Leptodactylus melanonotus.




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Advertisement call. Dominant frequency (either funda-

mental frequency or first harmonic) 1,000–1,500 Hz or

2,000–3,000 Hz; note duration 0.02–0.09 s; weak falling

frequency modulations; each call consisting of one or two

pulsed notes; call rate 150–160/min; harmonic structure

usually present (Heyer, 1970a:31–32; Straughan and

Heyer, 1976:227) (Fig. 114).

Distribution. Lowland Atlantic and Pacific coasts of

Mexico through Panamá and wet Pacific lowlands of Co-

lombia and Ecuador (Fig. 115).

Leptodactylus natalensis Lutz, 1930 (Plate 11C)

Leptodactylus natalensis Lutz, 1930:7. Type locality: “Na-

tal, Rio Grande do Norte. Rio Baldo e outros lugar-

es,” Brazil [Portuguese text]; “Rio Bahú and other

places near Natal [Rio Grande do Norte]” [English

text]. Heyer and Heyer, 2006b:3, suggested that

the type locality is “Rio Baldum, 06°09’S, 35°08’W.”

Syntypes: Including USNM 81130 according to Co-

chran, 1961:64; USNM 81130 designated lectotype

by Heyer, 1970a:22.

Etymology. The name alludes to the general locality (Na-

tal, Brazil) where the species was initially collected.


33.1–48.9 mm (X = 40.0 mm), male SVL 28.7–42.1 mm


with 2 keratinized spines on each thumb; males lacking

chest spines; a light stripe extending from under eye to

below the tympanum, sometimes interrupted or continu-

ous with a light commissural gland stripe; no dorsal folds;

dorsolateral folds absent (2%), short (46%), or moderate

length (53%); lateral folds absent; posterior thigh rarely

with distinct light stripes (5%), otherwise (95%) stripes

indistinct, usually(79%) light stripes indiscernible; up-

per shank barred; belly rarely lacking melanophores (1%),

usually lightly mottled (43%), moderately mottled (47%),

or rarely extensively mottled (9%); toes with lateral fring-

es (Heyer 1994:89–91; Heyer and Heyer 2006b:1).

Similar species. The only other Leptodactylus species

with toe fringing that occur with L. natalensis are L. la-

trans complex species and L. podicipinus. Leptodactylus

natalensis lacks dorsal folds; the members of the L. la-

trans complex have dorsal folds. Leptodactylus natalensis

lack distinct light belly spots; L. podicipinus often (42% of

specimens) have a spotted belly. Just over half of L. na-

talensis specimens have toe tips larger than narrow or

just-swollen categories; all L. podicipinus have either nar-

row or just-swollen toe tips.


39/40) 28 mm; oral disk anteroventral; tooth row formula

2/3; tail uniformly dark (Heyer and Heyer, 2006b:1–2).

Advertisement call. Beginning call/note dominant

(= fundamental) frequency ranging from 550–1,040 Hz to

final frequencies of 1,370–1,830 Hz; note duration 0.06–

0.07 s; notes pulsed, from 2–7 (modally 7) pulses or par-

tial pulses per note; rapidly rising frequency modulations

throughout call; call rate 3.0–4.1/s; harmonics present or

indiscernible (Amorim et al., 2009:1–7; Heyer and Car-

valho, 2000:284–289; Heyer and Heyer, 2006b:2; Prado

et al., 2007:97–103) (Fig. 116).

Distribution. Leptodactylus natalensis occurs in the Bra-

zilian State of Maranhão (Leite Jr. et al., 2008:153–156),

northern and central portions of the Brazilian Atlantic

Forest Morphoclimatic Domain (Ab’Sáber, 1977) from its

most northern extent in the State of Rio Grande do Norte

to and including the State of Rio de Janeiro (Fig. 117).

Figure 116. Advertisement call of Leptodactylus natalensis (recording

USNM 323).

Figure 117. Distribution map of Leptodactylus natalensis.




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Leptodactylus nesiotus Heyer, 1994 (Plate 11D)

Leptodactylus nesiotus Heyer, 1994:91. Type locality:

“Trinidad; St. Patrick; Icacos Peninsula, Icacos.” Ho-

lotype: USNM 306179, adult male.

Etymology. From the Greek nesiotes, islander, in reference

to its only known occurrence on the Island of Trinidad.

Adult morphology. Small, male SVL 31.7–33.0 mm

(n = 3); adult male snout not spatulate; distinct broad

light upper lip stripe present; males with two small black

spines on thumb; males lack chest spines; no dorsal folds;

weakly developed dorsolateral folds from posterior eye

to sacrum; lateral folds absent; posterior thighs with or

without light stripes; upper shank barred; belly speckled;

toes with lateral fringes (Heyer, 1994:91). Osteology was

described by Ponssa et al. (2010).

Similar species. Leptodactylus nesiotus is known only

from Trinidad, where L. insularum and L. validus are the

only other Leptodactylus with toe fringes. Leptodactylus ne-

siotus is a small species (males 32–33 mm SVL) with mod-

erate-length, interrupted dorsolateral folds; L. insularum

is a moderate/large species (males to 88 mm SVL, males

to 94 mm SVL) with long, complete dorsolateral folds.

Leptodactylus nesiotus has a broad light stripe on the en-

tire upper lip or at least to under the eye; in individuals

of L. validus with discernible light lip stripes, the stripes

extend from the posterior corner of the eye posteriorly.



quency 1,500–2,000 Hz; call duration 0.03 s; calls with

4–5 partial pulses; calls frequency modulated with fast

rise times; call rate ca. 3.8 calls per second; harmonic

structure ambiguous (Heyer, 1994:94) (Fig. 118).

Distribution. Icacos Peninsula, Trinidad (Fig. 119).

Leptodactylus pascoensis Heyer, 1994

Leptodactylus pascoensis Heyer, 1994:94. Type local-

ity: “Perú; Pasco; Iscozazin Valley, Contilla, 780 m,

≈ 10°17’S, 75°13’W.” Holotype: LACM 40665, adult

male.

Etymology. Named for the Peruvian department of Pasco

where most of the known specimens have been collected.


66.6 mm (X = 59.3 mm), male SVL 60.3–61.4 mm

(X = 60.7 mm); male snout not spatulate; adult males

with a pair of large black thumb spines; males lacking

chest spines; somewhat distinct light stripe from poste-

rior corner of eye passing under tympanum through jaw

commissure or indiscernible light upper lip stripe; dorsal

folds absent; dorsolateral folds absent, short, or medium

length; lateral folds absent; posterior thigh light stripe

indistinct or usually indiscernible; upper shank weakly

cross-banded; belly lightly to moderately mottled; toes


Similar species. Leptodactylus pascoensis occurs in a re-

stricted region along the Amazonian flanks of the An-

des in central Perú, Departments of Huanuco and Pasco.

Other Leptodactylus with toe fringes that may occur with

L. pascoensis are L. bolivianus, L. diedrus, L. griseigularis,

L. latrans complex species, L. leptodactyloides, L. petersii,

and L. wagneri. Both Leptodactylus bolivianus and L. la-

trans complex species have distinct, complete dorsolat-

eral folds; L. pascoensis does not have complete distinct

dorsolateral folds. Leptodactylus pascoensis is larger than

L. diedrus (L. pascoensis females 52–67 mm SVL, males

60–61 mm SVL; L. diedrus females 34–48 mm SVL, males

30–40 mm SVL); the ventral and posterior thigh patterns

merge in L. pascoensis whereas they abut in L. diedrus. Lep-

todactylus pascoensis is larger than L. griseigularis (female

Figure 118. Advertisement call of Leptodactylus nesiotus.

Figure 119. Distribution map of Leptodactylus nesiotus.




S79


L. griseigularis 35–59 mm SVL, males 34–53 mm SVL.

Leptodactylus latrans complex species have distinct, com-

plete dorsolateral folds; L. pascoensis dorsolateral folds

are not distinct and complete; Leptodactylus pascoensis is

larger than L. leptodactyloides (female L. leptodactyloides

35–56 mm SVL, males 28–48 mm SVL); most L. pascoen-

sis individuals have mottled posterior thigh surfaces with

no indication of light stripes, whereas L. leptodactyloides

individuals usually have at least some indication of light

posterior thigh stripes. Leptodactylus pascoensis is larger

than L. petersii (L. petersii females 31–51 mm SVL, males

27–41 mm SVL) and the belly is never extensively mot-

tled in an anastomotic pattern whereas most L. petersii

have extensively patterned bellies and often with an anas-

tomotic pattern. Leptodactylus pascoensis lack dorsolateral

folds extending from posterior to the eye to the sacrum;

L. wagneri most commonly have dorsolateral folds extend-

ing from the eye to the sacrum. The bellies of L. pascoensis

are lightly to moderately mottled, but never boldly mot-

tled; the bellies of most L. wagneri are moderately mottled

and some are extensively mottled with a bold pattern, ap-

proaching an anastomotic configuration.



Distribution. Central Peru east of the Andes between

780–2500 m (Fig. 120).

Leptodactylus petersii (Steindachner, 1864)

(Plate 11E)

Platymantis petersii Steindachner, 1864:254. Type local-

ity: “Marabitanas” Amazonas, Brazil. Holotype:

NMW lost according to Heyer, 1970a:17. Neotype

designation of AMNH 23182 by Heyer, 1970a:21

considered invalid by Heyer, 1994:79.

Leptodactylus brevipes Cope, 1887:51. Type locality: “at or

near … Chupada [= Chapada dos Guimarães], thirty

miles north-east of Cuyabá, and near the headwaters

of the Xingu, an important tributary of the Amazon,”

Mato Grosso, Brazil. Holotype: ANSP 11270, female.

Leptodactylus intermedius Lutz, 1930:8, 27. Syntypes:

AL-MN 1438–1441. Type locality: “Manacapuri

[= Manacapurú] perto do Manaos,” Amazonas, Bra-

zil [Portuguese text]; “Manacapuri near Manaos”

Brazil [English text]).

Leptodactylus (Platymantis) petersii: Lutz, 1930:1, 21.

Leptodactylus caliginosus petersi [sic]: Parker, 1935:507.

Leptodactylus podicipinus petersii: Gans, 1960:305.

Leptodactylus petersii: Rivero, 1961:48.

Etymology. Dr. Franz Steindachner described Platyman-

tis petersii in honor of Dr. Wilhelm Carl Hartwig Peters, a

prolific herpetologist, who was the Director of the Zoolo-

gisches Museum in Berlin for over 25 years.

Adult morphology. Small to moderate size, female SVL

31.2–51.3 mm (X = 39.2 mm), male SVL 26.6–41.1 mm

(X = 32.9 mm); adult snout not spatulate; males with a

pair of black spines on each thumb; males lacking chest

spines; light upper lip stripes extending from posterior

corner of eye distinct to not discernible; dorsal folds

absent; dorsolateral folds absent, short, or of moderate

length, interrupted; lateral folds absent; posterior thigh

light stripes usually absent (90% of specimens); upper

shank barred, belly usually extensively mottled (66%);

toes with lateral fringes (Heyer, 1994:96–97).

Similar species. Leptodactylus petersii occurs in greater

Amazonia and the Guiana shield region. The other Lepto-

dactylus species with toe fringes that occur with L. petersii

are L. bolivianus, L. diedrus, L. griseigularis, L. guianensis,

L. leptodactyloides, L. pascoensis, L. podicipinus, L. riveroi,

L. sabanensis, L. validus, and L. wagneri. Leptodactylus

petersii is smaller than L. bolivianus, L. guianensis, and

L. riveroi (L. petersii females 31–51 mm SVL, males 27–

41 mm SVL; L. bolivianus females 61–108 mm SVL, males

79–122 mm SVL; L. guianensis females 66–109 mm SVL,

males 80–110 mm SVL; L. riveroi females 57–89 mm SVL,

males 42–64 mm SVL), and L. petersii individuals have

at most a pair of medium-length, distinct dorsolateral

folds whereas all L. bolivianus, L. guianensis, and L. riv-

eroi have a pair of distinct dorsolateral folds extending

from eye to groin. The belly of L. petersii usually is ex-

tensively mottled (66%), whereas the belly of L. diedrus

usually lacks melanophores. In addition, the ventral and

posterior thigh patterns merge in L. petersii, whereas they

abut in L. diedrus. Leptodactylus petersii is smaller than

Figure 120. Distribution map of Leptodactylus pascoensis.




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L. griseigularis (L. griseigularis females 39–58 mm SVL,

males 35–51 mm SVL). The commonest belly pattern in

L. petersii is an extensive mottle in an anastomatic pat-

tern, whereas in L. griseigularis it is a light mottle without

an anastomatic pattern. Leptodactylus petersii individuals

have relatively uniformly and extensively patterned bel-

lies, often in an anastomotic pattern; L. leptodactyloides

belly patterns are more developed anteriorly, and most

individuals have moderate mottling but not in an anas-

tomotic pattern. Most (90%) L. petersii lack distinct light

posterior thigh stripes; most L. leptodactyloides have dis-

tinct light posterior thigh stripes. Leptodactylus petersii

is smaller than L. pascoensis (L. pascoensis females 52–

67 mm SVL, males 60–61 mm SVL), and the belly is usu-

ally darker in L. petersii than in L. pascoensis (L. pascoensis

bellies are never extensively mottled nor in an anasto-

motic pattern). Leptodactylus petersii lack distinct light

spots on the belly, whereas the belly of L. podicipinus is

commonly and densely spotted. The commonest toe-tip

state in L. petersii is just swollen, and some individuals

have swollen and just-expanded toe tips; the commonest

toe tip state in L. podicipinus is narrow, and L. podicipinus

lack swollen or just expanded toe tips. Leptodactylus pe-

tersii is smaller than L. sabanensis (L. sabanensis females

42–57 mm SVL, males 35–46 mm SVL). Usually, L. peter-

sii (56%) have light chin/throat spots; few L. sabanensis

(15%) have light chin/throat spots, and no L. sabanensis

have anastomotic or speckled belly patterns. Leptodacty-

lus petersii bellies usually are extensively mottled; Lepto-

dactylus validus usually have lightly mottled bellies with

a pattern ranging from a fine mottle to distinct, rather

dark blotches, with the pattern usually more intensely de-

veloped anteriorly. Leptodactylus petersii is smaller than

L. wagneri (L. wagneri females 52–82 mm SVL, males

39–61 mm SVL) and L. petersii lack dorsolateral folds ex-

tending from eye to groin, whereas most L. wagneri have

them.



la 2(2)/3; tail almost uniformly brown or musculature

moderately mottled brown (Duellman, 2005:288; Heyer,

1994:96–97).

Advertisement calls. Call type 1 (Fig. 121A): Dominant

(= fundamental) frequency 700–1,200 Hz; call duration

0.04–0.05 s; calls of 3–4 partially pulsed notes; calls not

noticeably frequency modulated; call rate 2.9–4.2 notes/s;

harmonics weakly to strongly developed. Call type 2

(Fig. 121B): Calls of two juxtaposed notes. Dominant fre-

quency of first note 800–1,600 Hz, of second note 1,800–

2,800 Hz; call duration 0.03–0.05 s; first note of 2–4 par-

tial pulses, second note not noticeably pulsed; first note

frequency modulated upward with a fast rise time, sec-

ond note often frequency modulated downward; call rate

0.6–1.3 s; first note with harmonic structure, second note

apparently without harmonic structure (Heyer, 1994:97).

Distribution. Guianas, Amazon basin, and isolated gal-

lery forests in Cerrado open formations in central Brazil

(Fig. 122).

Figure 121. Advertisement call of Leptodactylus petersii. (A) Call type

1. (B) Call type 2.

Figure 122. Distribution map of Leptodactylus petersii (recording

USNM 207).




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Leptodactylus podicipinus (Cope, 1862) (Plate 11F)

Cystignathus podicipinus Cope, 1862:156. Type locality:

“Paraguay.” Type: ANSP 14539, female. USNM 5831

marked in ledger as “Type.” Remark in USNM ledger

states: “Type now in ANS[P], 14539. See Dunn’s list.”

Leptodactylus podicipinus: Boulenger, 1882:248.

Leptodactylus nattereri Lutz, 1926b:1011. Type locality:

“la station de Ilha Sêca (Chemin de fer Noroeste do

Brazil. Etat de S[ão]. Paulo” and “Cachoeira do Mari-

bondo, … Etat de S[ão]. Paulo,” Brazil. Syntypes:

AL-MN 1314–15 (plus unnumbered specimen in

same jar). Synonymy by Cochran, 1955 “1954”:326.

Leptodactylus podicipinus podicipinus – Gans, 1960:305.

Etymology. From the Greek podicus (belonging to a foot)

and pinos (dirt).


29.3–54.0 mm (X = 38.8 mm), male SVL 24.5–43.3 mm

(X = 34.0 mm); adult snout not spatulate; males with a

pair of keratinized spines on thumb; males lack chest

spines; light upper lip stripe distinct (22% of specimens),

indistinct (43%) or absent (35%); dorsal folds absent; dor-

solateral folds absent (9%), short (44%), moderate (46%),

or extending from eye to groin (1%); lateral folds absent;

posterior thighs usually completely mottled with no indi-

cation of light stripes (79%), stripes sometimes indistinct

(17%), or stripes rarely distinct (4%); upper shank barred;

distinct light spots on belly (42%), otherwise light to dark

profusion of melanophores; toes with lateral fringes (Hey-

er, 1994:97–99).

Similar species. Other species with toe fringes that oc-

cur sympatrically with L. podicipinus are L. bolivianus,

L. diedrus, L. griseigularis, L. latrans complex species,

L. leptodactyloides, L. natalensis, L. petersii, L. pustula-

tus, and L. riveroi. Leptodactylus podicipinus is smaller

than L. bolivianus and L. riveroi (L. podicipinus females

30–54 mm SVL, males 24–43 mm SVL; L. bolivianus fe-

males to 88 mm SVL, males to 94 mm SVL; L. riveroi

females to 81 mm SVL, males to 63 mm SVL); dorso-

lateral folds are poorly developed and rarely long in

L. podicipinus, whereas dorsolateral folds in all L. bo-

livianus and L. riveroi extend from eye to groin and are

well-developed. The bellies of L. podicipinus usually are

extensively mottled and the ventral and posterior thigh

patterns merge; the bellies of L. diedrus usually lack me-

lanophores and the ventral and posterior thigh patterns

abut. Leptodactylus podicipinus is smaller than L. grisei-

gularis (L. griseigularis females 39–58 mm SVL, males

35–51 mm SVL) and the bellies of L. podicipinus are usu-

ally darker than those of L. griseigularis; L. griseigularis

bellies are usually lightly mottled and no individuals

have light belly spots. Leptodactylus podicipinus lacks

dorsal folds; L. latrans complex specimens have a pair

of dorsal folds. The posterior thighs of most L. podicipi-

nus are mottled with no indication of light stripes and

L. podicipinus usually have distinct light belly spots; the

commonest posterior thigh state in L. leptodactyloides

is a distinct stripe and L. leptodactyloides lacks distinct

light belly spots. All L. podicipinus have either narrow

or just-swollen toe tips and often have distinct light

belly spots; just over 50% of all L. natalensis have toe

tips larger than just swollen toe tips, and no L. natalen-

sis have distinct light belly spots. All L. podicipinus have

narrow or just-swollen toe tips and often have distinct

Figure 123. Advertisement call of Leptodactylus podicipinus.

Figure 124. Distribution map of Leptodactylus podicipinus.




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light belly spots; the commonest toe tip state in L. pe-

tersii is just swollen and some individuals have swollen

and just-expanded toe tips and no L. petersii have dis-

tinct light belly spots. No L. podicipinus have discrete,

distinct light spots on the posterior face of the thigh;

all L. pustulatus do.



2(2)/3; tail uniform brown or brown with few small light

specks (Rossa-Feres and Nomura, 2006: unnumbered

pages 8, 20; Vizotto, 1967:109–112).


quency 1,000–3,500 Hz; call duration 0.02–0.04 s; calls

with 3–7 pulses/partial pulses; rising frequency modula-

tions; call rate 0.5–8.4/s; harmonics weakly to moderately

developed (Guimarães et al., 2001:9; Heyer, 1994:99; Sil-

va et al., 2008:123–134) (Fig. 123).

Distribution. Open formations of Paraguay, adjacent Ar-

gentina, Bolivia, northwestern Uruguay, and central Bra-

zil, extending along the Rio Madeira and Rio Amazonas

within the Amazon Basin (Fig. 124).

Leptodactylus pustulatus (Peters, 1870) (Plate 12A)

Entomoglossus pustulatus Peters, 1870:647. Type locality:

“Ceara [Nördl. Brasilien],” northeastern Brazil. Holo-

type: ZMB 6951 according to Bauer et al., 1995:45.

Heyer, 1970a:16, incorrectly reported the type as

lost and designated MCZ 373 as neotype).

Leptodactylus pustulatus: Boulenger, 1882:239.

Etymology. From the Latin pustulatus, blistered, refer-

ring to the rough texture of the dorsum.


61.0 mm (X = 50.4 mm), male SVL 33.1–47.7 mm


lacking thumb and chest spines; light upper lip stripe

absent (area behind eye may be light); dorsal folds ab-

sent; dorsolateral folds interrupted or absent; lateral

folds interrupted or absent; posterior thigh almost

always with large, light spots, no light stripe; up-

per shank almost uniform dark; belly dark with large,

discrete light spots; toes with lateral fringes (Heyer,

1970a:16–17).

Similar species. Leptodactylus pustulatus occurs in the

Brazilian states of Ceará, Goiás, Mato Grosso, Pará, and

Tocantins. The other species most similar to L. pustu-

latus that have fringed toes and dorsolateral folds that

are interrupted or absent and co-occur with L. pustula-

tus are L. leptodactyloides, L. petersii, and L. podicipinus.

Leptodactylus pustulatus has large discrete light spots on

the belly and posterior thigh; Leptodactylus leptodactyloi-

des and L. petersii lack light spots on the belly; L. podicipi-

nus often has small light belly spots and no distinct light

spots on the posterior thighs.

Larval morphology. Total length (Gosner 39) 30.2 mm;

oral disk anteroventral; tooth row formula 2(2)/3; tail

dark gray (de Sá et al., 2007a:49–58).


quency 775–861 Hz; call duration 0.081–0.088 s; call

of two notes, each pulsed; rising and falling frequency

modulations throughout call; call rate 26/min; harmonic

structure variable throughout call (Brandão and Heyer,

2005:566–570) (Fig. 125).

Distribution. Arid and semi-arid habitats in central and

northeastern Brazil (Fig. 126).

Figure 125. Advertisement call of Leptodactylus pustulatus (recording

USNM 330).

Figure 126. Distribution map of Leptodactylus pustulatus.




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Leptodactylus riveroi Heyer and Pyburn, 1983

(Plate 12B)

Leptodactylus riveroi Heyer and Pyburn, 1983:560. Type lo-

cality: “Colombia; Vaupés, Timbó, 01°06’S, 70°01’W,

elevation 170 m.” Holotype: USNM 232400, male.

Etymology. Named for Dr. Juan A. Rivero “in recognition

of Dr. Rivero’s [numerous frog systematic and distribu-

tion] contributions.”


89.0 mm (X = 72.5 mm), male SVL 42.1–63.5 mm


with a pair of black thumb spines; males lacking chest

spines; distinct light stripe from under eye to tympanum;

dorsal folds absent; distinct pair of dorsolateral folds; lat-

eral folds absent; posterior thigh lacking light stripe; up-

per shank variegated or with transverse bars; belly boldly

mottled; toes with lateral fringes (Heyer and Pyburn,

1983:560–566).

Similar species. Leptodactylus riveroi occurs in Amazo-

nian drainages of Colombia and Venezuela and the states

of Amazonas and Pará in Brazil. Similar species with well

defined complete dorsolateral folds and toe fringes that

occur with L. riveroi are L. bolivianus, L. guianensis, L. la-

trans complex, and L. leptodactyloides. Leptodactylus riv-

eroi have complete black-bordered dorsolateral folds and

adult males lack chest tubercles; L. bolivianus and L. guia-

nensis have interrupted dark borders next to the dorso-

lateral folds and sexually active adult male L. bolivianus

and L. guianensis have patches of chest tubercles. Lepto-

dactylus riveroi lacks dorsal folds; L. latrans complex spe-

cies have dorsal folds. Leptodactylus riveroi has complete

dorsolateral folds; L. leptodactyloides dorsolateral folds are

interrupted, short to long.



2(2)/3; up to stage 37, tails transparent brown, beyond

stage 37, tails black (Lima, 1992:91–93).

Advertisement call. Dominant frequencies range from

360–830 Hz; call duration 0.7–2.3 s; each call of 9–28

double-pulsed notes; falling and rising frequency modula-

tions within notes; call rate about 2 per s; no harmonic

structure (Heyer and Pyburn, 1983:563–564) (Fig. 127).

Distribution. Amazonian drainages in Colombia and

Venezuela and the states of Amazonas and Pará in Brazil

(Fig. 128).

Leptodactylus sabanensis Heyer, 1994 (Plate 12C)

Leptodactylus sabanensis Heyer, 1994:99. Type locality:

“Venezuela; Bolívar; km 127, El Dorado–Santa Ele-

na de Uairen [= Vairen] road, 1250 m, ≈ 06°00’N,

61°30’W.” Holotype: KU 166559, adult male.

Etymology. “Named to indicate this species is geographi-

cally centered on the Gran Sabana of Venezuela.”


56.9 mm (X = 51.0 mm), male SVL 35.0–46.4 mm


males with a pair of medium to large black thumb spines;

males without chest spines; light upper lip stripe usual-

ly absent, if present extending from posterior corner of

eye to jaw commissure (15% of specimens); dorsal folds

absent; dorsolateral folds extending from eye to sacral

area or absent; lateral folds indistinct; posterior thigh

light stripe distinct (23% of specimens) to indistinct or

not discernible (77%); upper shank uniform to faintly

Figure 127. Advertisement call of Leptodactylus riveroi (recording

USNM 128).

Figure 128. Distribution map of Leptodactylus riveroi.




S84


barred; belly lightly (15% of specimens), moderately (61%

of specimens) or extensively (24% of specimens) mottled;

toes with lateral fringes (Duellman, 1997:26–27; Heyer,

1994:99–103).

Similar species. Leptodactylus sabanensis is known from

the Gran Sabana of Venezuela (State of Bolívar) and the

adjacent lavrado of the State of Roraima, Brazil. Similar

species having toe fringes in the distribution of L. saba-

nensis are L. guianensis, L. latrans complex species, L. pe-

tersii, and L. validus. Most L. sabanensis lack long complete

dorsolateral folds, if present, they are indistinct or inter-

rupted; L. guianensis has smooth, complete dorsolateral

folds. Leptodactylus sabanensis lacks dorsal folds; L. latrans

complex species has dorsal folds. Leptodactylus sabanen-

sis is larger than L. petersii (L. petersii females 31–51 mm

SVL, males 27–41 mm SVL), few L. sabanensis (15%) have

light chin/throat spots, and L. sabanensis have a lightly to

extensively mottled belly pattern; most (56%) L. petersii

specimens have light chin and throat spots and an anas-

tomotic or speckled belly pattern; L. sabanensis do not

have anastomotic or speckled belly patterns that char-

acteristically occur in L. petersii. Leptodactylus sabanensis

is larger than L. validus (female L. validus 29.5–51.5 mm

SVL, males 27.8–42.9 mm SVL); the most common upper

lip stripe condition in L. sabanensis is indiscernible (when

discernible, the light stripes extend from the posterior

corner of the eye); the commonest upper lip stripe condi-

tion in mainland L. validus is distinct light stripes that of-

ten extend posteriorly from under the middle of the eye.



mula 2(1)/3[1]; tail brown with white flecks (Duellman,

1997:27).


quency 1,400–1,800 Hz; call duration 0.04–0.06 s; call

slightly pulsed; rising frequency modulations through-

out call; call rate 1.2/s; weak harmonic structure (Heyer,

1994:54, 102) (Fig. 129).

Distribution. Gran Sabana of Venezuela and adjacent

Lavrado in Roraima, Brazil (Fig. 130).

Leptodactylus validus Garman, 1888 (Plate 12D)

Leptodactylus validus Garman, 1888 “1887”:14. Type

locality: “Kingston, St. Vincent,” Lesser Antilles.

Syntypes: MCZ 2185 (42 specimens, according to

Barbour and Loveridge, 1929:294), ANSP 19425

and 26108 (according to Malnate, 1971:353), and

UMMZ 55761 (3 specimens, according to Peters,

1952:19); MCZ 71920 designated lectotype by Hey-

er, 1970a:21; see Comments, below.

Leptodactylus pallidirostris Lutz, 1930:1–20. Type locality:

“Kartarbo [= Kartabo],” Guyana. Syntypes: AL-MN

1829 adult male designated lectotype by Heyer,

1994:93. Synonymy by Yanek, Heyer, and de Sá,

2006:192.


29.5–51.5 mm (X = 38.4 mm), male SVL 27.8–42.9 mm


males with a pair of black thumb spines; males lacking

chest spines; distinct light upper lip stripes originating

from the posterior corner of the eye and extending pos-

teriorly or indiscernible; dorsal folds absent; dorsolateral

folds usually short, rarely absent or rarely ½ distance from

posterior eye to groin; lateral folds absent; posterior thigh

with distinct to indiscernible light stripe; upper shank

lightly barred or uniform; belly mottled; toes with lateral

fringes (Heyer, 1994:93–94, 102–104).

Similar species. Leptodactylus validus is the only Lep-

todactylus species with lateral toe fringes that occurs in

the Lesser Antilles. On the islands of Trinidad and To-

bago, L. validus occurs with fringe-toed L. insularum and

Figure 129. Advertisement call of Leptodactylus sabanensis (recording

USNM 225).

Figure 130. Distribution map of Leptodactylus sabanensis.




S85


L. nesiotus. eptodactylus validus does not have complete

dorsolateral folds, L. insularum does. In individuals of

L. validus with light upper lip stripes, the light lip stripes

extend posteriorly from the posterior corner of the eye.

Leptodactylus nesiotus has a broad light stripe on the en-

tire upper lip or at least to under the eye. Mainland South

American Leptodactylus validus occur in the Guiana shield

region. Other species of Leptodactylus that occur in the

same area with toe fringes are L. diedrus, L. guianensis,

L. latrans complex species, L. leptodactyloides, L. peter-

sii, and L. sabanensis. Some individuals of L. validus lack

dorsolateral folds and the ventral and posterior thigh

patterns merge; all L. diedrus lack dorsolateral folds and

the ventral and posterior thigh patterns abut. Mainland

L. validus have short to medium dorsolateral folds; L. gui-

anensis have dorsolateral folds that extend from behind

the eye posteriorly to the groin. Leptodactylus validus

lacks dorsal folds; L. latrans complex species have com-

plete dorsal folds. Mainland L. validus are smaller than

L. leptodactyloides (L. leptodactyloides females 35–56 mm

SVL, males 28–48 mm SVL) and are commonly charac-

terized by an upper lip stripe that extends extends pos-

teriorly from the middle of the eye and light chin/throat

spots; L. leptodactyloides usually have indistinct upper lip

stripes that extend from the posterior corner of the eye

and few L. leptodactyloides have light chin/throat spots.

Many L. validus individuals have light chin/throat spots;

few L. leptodactyloides do. The belly of L. validus usually

is lightly mottled with patterns ranging from a fine mot-

tle to distinct, rather dark blotches and the commonest

toe-tip condition in L. validus is swollen with some indi-

viduals having expanded tips or small disks; the belly of

L. petersii usually is extensively mottled, often in an anas-

tomotic pattern, and the commonest toe-tip condition in

L. petersii is just swollen and no individuals have expanded

toe tips or small toe disks. Leptodactylus validus is smaller

than L. sabanensis (L. sabanensis females 42–57 mm SVL,

males 35–46 mm SVL), the upper lip stripe of L. validus is

distinct and extends posteriorly from under the middle

of the eye and its advertisement call broadcast frequency

ranges from 1,500–3,500 Hz with a maximum energy of

2,500–3,500 Hz; the most common upper lip stripe condi-

tion in L. sabanensis is indiscernible, and, when lip stripes

are discernible, they extend from the posterior corner of

the eye; the broadcast frequency range of the advertise-

ment call of L. sabanensis is 900–2,300 Hz with maximum

energy of 1,400–1,800 Hz.

Larval morphology. Based on St. Vincent larvae. Maxi-

mum total length (Gosner 36) 25.8 mm; oral disk antero-

ventral; tooth row formula at Gosner stage 25, 2(2)/3,

Gosner stages 29–38, 2/3; tail gray with heavy profusion

of melanophores on entire tail except for a large very dis-

tinct to indistinct light spot over anterior tail muscula-

ture (Heyer, 1994:104).

Advertisement call. Call data from mainland and is-

land populations are very similar (Yanek et al., 2006),

both consisting of two notes. The first note consists of

a single pulse and calls have fast rising frequency modu-

lations throughout. Call differences were reported be-

tween mainland and island populations (Heyer, 1994,

figs. 27–29, 31–33). The differences are in mainland pop-

ulations having (1) dominant broadcast frequency range

1,500–3,500 Hz (2,300–3,500 Hz for island populations),

(2) call duration 0.03–0.05 s (0.03–0.06 for island popu-

lations), (3) second note with 2–5 pulses (2–6 pulses for

island populations), (4) and call rate 0.8–2.7/s (call rate

1.1–1.9/s for island populations) (Fig. 131).

Distribution. Guiana shield region, Trinidad, Tobago,

and Lesser Antilles (Fig. 132).

Comments. Designation of a lectotype for Leptodactylus

validus has a tortuous history. Garman’s (1888 “1887”)

original description did not specify how many specimens

Figure 131. Advertisement call of Leptodactylus validus.

Figure 132. Distribution map of Leptodactylus validus.




S86


were syntypes. He did not designate any of the specimens

as types nor did he provide any museum numbers for the

frogs. The only information relating to the frogs of the

new species is: “A male measures in length of body one

and five–eighths inches and in leg two and three–eighths;

a female is one and three-fourths in body and two and a

half inches in length of leg.”

Barbour and Loveridge (1929:294) stated that the

type specimens of Leptodactylus validus comprised a lot of

42 specimens (all assigned the same MCZ catalogue num-

ber 2185). Two syntypes were deposited in the Academy

of Natural Sciences at Philadelphia (ANSP 19425, 26108).

Heyer (1970a:21) designated the first lectotype: “I

hereby designate MCZ 71920, an adult male, from Kings-

ton, St. Vincent, as the lectotype of Leptodactylus validus

Garman.” Subsequently, Schwartz and Thomas (1975:44)

stated: “Heyer (op. cit. [1970a]:21) designated MCZ

71920 as lectotype of L. validus, but since this specimen is

not part of the syntypic series the designation is invalid.”

Heyer (1994:80) seemingly ignored some of the pre-

ceding history when he wrote: “Garman described L. vali-

dus on the basis of three specimens, ANSP 19425, 26108,

and MCZ 2185 from Kingston, St. Vincent. Schwartz and

Thomas (1975:44) pointed out that my previous designa-

tion of MCZ 71920 as the lectotype (Heyer, 1970a:21) was

invalid, as MCZ 71920 was not part of the syntypic series.

In my folder of data and photographs of Leptodactylus

types, I have written on the back of the photograph of the

frog, ‘L. validus Garman Lectotype MCZ 2185,’ Why I have

the correct number in my type file but cited an incorrect

number in the publication is a mystery at this point. MCZ

2185 is an adult male in good condition, and as the Gar-

man article refers to specimens in the Museum of Com-

parative Zoology, it is appropriate to designate MCZ 2185

as the lectotype of Leptodactylus validus Garman.”

E-mail correspondence with Jose Rosado, MCZ (22

July 2010) clarifies the situation: “Your ‘error’ [Heyer

1970a:102{sic, correct page is 21}] as such may not be

a mistake after all because MCZ A-71920 is part of the

syntypic series. … Schwartz and Thomas may never have

checked the actual situation. The original catalogue en-

try indicated that we had 57 specimens listed under MCZ

A-2185, B and L [Barbour and Loveridge, 1929] listed

42 remaining in the collection in 1929, at present there

are 40. You are correct in that the ‘duplicates’ were re-

catalogued and the original number MCZ A-2185 was

arbitrarily assigned to the adult male. The remaining

specimens were retagged and given the numbers MCZ

A-71920–71958, so your designation is correct. Schwartz

and Thomas were just not informed.”

Consequently, herein it is considered that the first

designation for the lectotype of Leptodactylus validus,

MCZ A-71920 by Heyer (1970a:21) takes priority over

Heyer’s (1994:80) subsequent lectotype designation of

MCZ A-2185.

Leptodactylus wagneri (Peters, 1862) (Plate 12E)

Plectromantis wagneri Peters, 1862:232. Type locality:

Published originally “an den Westseite der Anden in

Ecuador” but data associated with the lost type spec-

imen was “Pastassathal” [= Pastaza Valley], Ecuador;

by neotype designation of Heyer, 1970a:39, the type

locality became Pastaza, Ecuador, on the east side of

the Andes. Neotype designation rejected by Heyer

(1994); consequently the type locality reverts to the

original statement by Peters. Type[s]: ZSM 1080/0,

lost according to Heyer, 1970a:19 and Glaw and

Franzen, 2006:174; neotype designated by Heyer,

1970a:19, as NRM 1945 [holotype of Eleutherodacty-

lus leptodactyloides]). This neotype designation con-

sidered invalid by Heyer, 1994:78, who determined

that Eleutherodactylus leptodactyloides and Plectro-

mantis wagneri represented different species.

Leptodactylus wagneri: Nieden, 1923:479.

Leptodactylus (Plectromantis) wagneri: Lutz, 1930:1, 21.

Etymology. Named for the collector, Dr. Moritz Wagner.


81.7 mm (X = 65.7 mm), male SVL 39.1–60.7 mm


with a pair of black thumb spines; males without chest

spines; light upper lip stripe distinct to not discernible;

dorsal folds absent; dorsolateral folds usually extending

from eye to groin; lateral folds absent; posterior thigh light

stripe distinct to not discernible; upper shank uniform to

barred; belly moderately mottled, sometimes boldly mot-

tled; toes with lateral fringes (Heyer, 1994:103–105).

Similar species. Leptodactylus wagneri occurs along the

Amazonian flanks of the Andes and is known to occur with

or in the same general region as the following Leptodacty-

lus species with toe fringes: L. bolivianus, L. colombiensis,

L. diedrus, L. discodactylus, L. griseigularis, L. latrans com-

plex species, L. leptodactyloides, L. pascoensis, and L. peter-

sii. Leptodactylus wagneri (female SVL 52–82 mm, male

SVL 39–61 mm) does not reach the same size as L. bolivi-

anus (female SVL 61–108 mm, male SVL 79–122 mm; few

L. wagneri have distinct posterior lip stripes that extend

from the posterior corner of the eye; many (70%) L. bolivi-

anus have light stripes on the upper lip including under

the eye. Leptodactylus wagneri is larger than L. colombien-

sis (L. colombiensis females 40–62 mm SVL, males 36–

56 mm SVL), and most (96%) L. wagneri have dorsolateral

folds extending from eye to groin; only some L. colombien-

sis have dorsolateral folds extending from eye to groin.

Leptodactylus wagneri is larger than L. diedrus (L. diedrus

females 34–48 mm SVL, males 30–40 mm SVL), and the

ventral and posterior thigh patterns merge in L. wagneri;

the ventral and posterior thigh patterns abut in L. diedrus.




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Leptodactylus wagneri does not have expanded toe tips

with dorsal grooves; L. discodactylus has expanded toe tips

with dorsal grooves. Leptodactylus wagneri is larger than

L. griseigularis (L. griseigularis females 35–59 mm SVL,

males 34–53 SVL) and the dorsolateral folds of L. wag-

neri commonly extend from behind the eye to the groin,

whereas the most common fold condition in L. griseigula-

ris is moderate (fold not reaching groin); the most common

belly pattern is lightly mottled in L. griseigularis and the

most common belly pattern is moderately to boldly mot-

tled in L. wagneri. Leptodactylus wagneri lacks dorsal folds;

L. latrans complex species have dorsal folds. Leptodactylus

wagneri is larger than L. leptodactyloides (L. leptodactyloi-

des females 35–56 mm SVL, males 28–48 mm SVL); most

L. wagneri have dorsolateral folds extending from eye to

groin; few L. leptodactyloides have folds extending from

eye to groin. Many L. wagneri have moderately to boldly

mottled bellies, whereas the bellies of L. leptodactyloides

characteristically are finely mottled. Leptodactylus wagneri

have boldly mottled and moderately mottled bellies; the

bellies of L. pascoensis are lightly to moderately, but never

boldly mottled. Leptodactylus wagneri is larger than L. pe-

tersii (females 31–51 mm SVL, males 27–41 mm SVL); the

dorsolateral folds of L. wagneri commonly extend from be-

hind the eye to the groin, no L. petersii have dorsolateral

folds extending from eye to groin.



Distribution. Amazonian slopes of the Andes in south-

ern Colombia, Ecuador, northern Perú, with a few records

from lowland Amazonia (Brazil, Colombia, Ecuador, Peru)

and a single specimen from the Pacific slopes in Colombia

(Fig. 133).

Leptodactylus species not assigned to a species

group

Leptodactylus hylodes (Reinhardt and Lütken,

1862)

Cystignathus hylodes Reinhardt and Lütken,

1862 “1861”:168. Type locality: Cotinguiba [now

Nossa Senhora do Socorro], Sergipe, Brazil; see Hey-

er, 2000 for clarification of type locality. Lectotype:

ZMUC R 11105, sex unclear, probably a juvenile.

Leptodactylus hylodes: Heyer, 2000:150–153.

Etymology. From the Greek hylodes, woody, bushy.

Morphology. Small, 25.3 mm (lectotype); snout not

spatulate; males without thumb or chest spines; upper

lip faintly barred; no visible dorsal, dorsolateral, or lateral

folds; light stripe on posterior thigh; upper shank barred;

belly uniform light; toes with well developed lateral fring-

es (Heyer, 2000).

Similar species. Leptodactylus hylodes is known only from

the type locality. One other species that occurs in the

same area is L. natalensis. Leptodactylus hylodes has het-

erogeneous fingertips with fingers II and III with round-

ed, non-expanded tips and fingers IV and V with small,

ungrooved disks, unique within Leptodactylus.

Figure 133. Distribution map of Leptodactylus wagneri. Figure 134. Distribution map of Leptodactylus hylodes.




S88




Distribution. Known only from the type locality

(Fig. 134).

Leptodactylus lauramiriamae Heyer and Crombie,

2005 (Plate 12F)

Leptodactylus lauramiriamae Heyer and Crombie,

2005:590. Type locality: “Brazil, Rondônia, north

end of the town of Vilhena, km 16, 12°43’S, 60°07’W

[coordinates for Vilhena]”. Holotype: MZUSP

132772, adult female.

Etymology. Named for a daughter of M.H. and W.R.

Heyer.


(X = 30.6 mm), male 32.3 mm; adult male snout spatu-

late; male lacking thumb spines and chest spines; light up-

per lip stripe absent; dorsal, dorsolateral, and lateral folds

absent; posterior thigh without light stripe; upper shank

barred; belly uniform light; toes without lateral fringes

(Heyer and Crombie, 2005:590–595).

Similar species. Leptodactylus lauramiriamae is unique in

the genus Leptodactylus in having an areolate belly.



Distribution. This rare species is known only from the

type material, an additional topotype (CHUNB 11921,

field label GRCOLLI 04689), and six uncataloged speci-

mens at MZUSP (LTT 39, 95, 101, 103, 105, and T 01)

from Tangará da Serra, Mato Gross, Brazil (14°37’10”S,

57°29’09”W) (Fig. 135).

Leptodactylus ochraceus Lutz, 1930

Leptodactylus ochraceus Lutz, 1930:28. Type locality: State

of Pernambuco (? Tapera), Brazil; see Caramas-

chi, 2008, for discussion of type locality. Holotype:

AL-MN 1445, female.

Etymology. From the Greek ochre, earthy oxide of iron.

Adult Morphology. Medium size, 41.7 mm SVL (Holo-

type), see below.



Distribution. Known only from the type locality.

Comments. The species was described based on a single

specimen by Lutz (1930); no other specimens have been

collected. Recently, Caramaschi (2008) examined the ho-

lotype and provided measurements and a description of

the current state of preservation (“poor condition, very

damaged”) and confirmed that the specimen is a female

by the presence of eggs; in addition, he reviewed histori-

cal data on the type locality. Caramaschi (2008) also de-

scribed and discussed the species morphology and color-

ation based on the illustration through examination of

the original plate. The holotype is a leptodactylid but can-

not be assigned to any of the 10 species of Leptodactylus

inhabiting the “Caatingas” domain of northeastern Brazil

(Caramaschi, 2008). The species has never been associ-

ated with any of the Leptodactylus species group.

ACKNOWLEDGMENTS

We thank the following individuals and institutions

for the loan of specimens, tissue samples, contribution to

field work, and/or providing working space at their collec-

tions: Reuber Brandão (UnB, Brazil), Janalee P. Caldwell Figure 135. Distribution map of Leptodactylus lauramiriamae.




S89


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(OSM, USA), Marta Canepa (FML, Argentina), Ulisses

Caramaschi (MNRJ, Brazil), Gustavo Carrizo (MACN, Ar-

gentina), Carolina Castro Mello (MZUSP, Brazil), Charles

Cole (AMNH, USA), Guarino Colli (UnB, Brazil), Luis Co-

loma (QCAZ, Ecuador), Celso Morato de Carvalho (INPA,

Brazil), Ignacio De la Riva (MNCN, Spain), Marcos Di

Bernardo (MCP, Brazil), Maureen Donnelly (FIU, USA), J.

Faivovich (MACN, Argentina), C.F.B. Haddad (UNESP, Rio

Claro, Brazil), James Hanken (MCZ, USA), David Kizirian

(AMNH, USA), Sonia Kretzschmann (FML, Argentina),

Esteban Lavilla (FML, Argentina), José Langone (MNHH,

Uruguay), John D. Lynch (ICN, Colombia), Raul Maneyro

(FC, Uruguay), Robert Murphy (ROM, Canada), José M.

Padial (Carniege Museum, USA), José Pombal Jr. (MNRJ,

Brazil), Ana Prudente (MPEG, Brazil), Steffen Reichle (Bo-

livia), José Rosado (MCZ, USA), Magno Segalla (Brazil),

Miguel Trefaut Rodrigues (USP, Brazil), Linda Trueb (KU,

USA), James I. Watling (FIU, USA), Jorge Williams (MLP,

Argentina), and Hussam Zaher (MZUSP, Brazil). We also

thank the individuals and MZUSP (listed in the plates

and back of front cover) who generously provided color

photos of species of Leptodactylus. Denis Jacob Machado,

Luis Lieu, Hussam Zaher, and the MZUSP Board of Di-

rectors were instrumental in installing and running the

high-performance computer cluster Ace. Maria L. Pons-

sa ackowledges support from Collection Study Grant

(AMNH), Ernst Mayr Grant (MCZ), and Short-Term Visi-

tor Program (SI), PICT 2008-578. Contributions to this

work by Arley Camargo, Maria L. Ponssa, Edward Stanley,

and Miriam H. Heyer (who assisted with published data

on Leptodactylus) were supported under NSF-DEB Award

DEB0342918. Taran Grant was supported by Conselho

Nacional de Desenvolvimento Científico e Tecnológico

Proc. 307001/2011-3 and Fundação de Amparo à Pesqui-

sa do Estado de São Paulo Proc. 2012/10000-5. This man-

uscript was completed under NSF-DEB award 1144692 to

Rafael O. de Sá.

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APPENDIX 1. GENBANK ACCESSION NUMBERS

Below we list the GenBank accession numbers of the DNA sequences included in the phylogenetic analysis of Leptodactylus.

New sequences are marked in boldface.

Terminal 12S 16S Rhodopsin

Adenomera hylaedactyla 1 DQ283063 DQ283063 DQ283790

Adenomera hylaedactyla 2 AY943240.1 AY943227 KM091505

Adenomera lutzi KM091597

Adenomera sp. AY364538 AY364538

Allophryne ruthveni AF364511, AF364512, AF843564 AF364511, AF364512, AF843564 AY844538

Alsodes gargola AY843565 AY843565 AY844539

Amazophrynella minuta AY843582 AY843582 AY844555

Atelognathus patagonicus AY843571 AY843571 AY844545

Atelopus spurrelli DQ502200 DQ502200

Batrachyla leptopus AY843572 AY843572 AY844546

Ceratophrys cranwelli AY843575 AY843575 AY843797

Chacophrys pierottii DQ283328 DQ283328

Craugastor rhodopis DQ283317 DQ283317 DQ283960

Crossodactylus schmidti AY843579 AY843579 AY844780

Cycloramphus boraceiensis DQ283097 DQ283097 DQ283813

Edalorhina perezi 1 AY843585 AY843585 AY844558

Edalorhina perezi 2 KM091465 KM091581 KM091515

Engystomops cf. freibergi DQ337229 DQ337229

Engystomops coloradorum DQ337222 DQ337222

Engystomops guayaco DQ337220 DQ337220

Engystomops montubio DQ337224 DQ337224

Engystomops petersi EF011554 EF011554

Engystomops pustulatus DQ337215 DQ337215

Engystomops pustulosus DQ337235 DQ337235

Engystomops randi DQ337228 DQ337228

Engystomops sp.B DQ337216 DQ337216

Engystomops sp.D DQ337218 DQ337218

Espadarana prosoblepon AY364358, AY364379, AY843574 AY364358, AY364379, AY843574 AY364404

Eupsophus calcaratus AY843587 AY843587 AY844560

Gastrotheca megacephala AY843592 AY843592 AY844564

Hemiphractus helioi AY843594 AY843594 AY844566

Hyalinobatrachium eurygnathum AY843595 AY844567

Hyalinobatrachium fleischmanni DQ283453 DQ283453 DQ284043

Hyalinobatrachium sp. AY326024 AY326024

Hydrolaetare caparu KM091473 KM091589 KM091526

Hydrolaetare dantasi KM091474 KM091590 KM091527

Hylodes phyllodes DQ283096 DQ283096 DQ283812

Hypsiboas boans AY843610 AY843610 AY844588

Lepidobatrachus laevis DQ283152 DQ283152 DQ283851

Leptodactylus albilabris KM091460 KM091577 KM091506

Leptodactylus bolivianus KM091461 HQ232831 KM091507

Leptodactylus bufonius AY943220 AY943233 KM091508

Leptodactylus camaquara KM091462 KM091578 KM091509

Leptodactylus chaquensis EF613179 EF632055 KM091510

Leptodactylus colombiensis KM091463 KM091579 KM091511

Leptodactylus cunicularis KM091464 KM091580 KM091512

Leptodactylus didymus AY948953 AY948957 KM091513

Leptodactylus diedrus AY943217 AY943230 KM091514

Leptodactylus discodactylus AY943226 AY943239




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Terminal 12S 16S RhodopsinLeptodactylus elenae KM091466 KM091582 KM091516Leptodactylus fallax KM091467 KM091583 KM091517Leptodactylus flavopictus KM091468 KM091584 KM091518Leptodactylus fragilis KM091469 KM091585 KM091519Leptodactylus furnarius KM091470 KM091586 KM091520Leptodactylus fuscus 1 AY911275Leptodactylus fuscus 2 AY905712 AY911281 KM091523Leptodactylus fuscus 3 AY905715 KM091522Leptodactylus fuscus 4 DQ283404 DQ283404 DQ284015Leptodactylus fuscus 5 AY911284Leptodactylus fuscus 6 AY905702 AY911271Leptodactylus fuscus 7 AY905705 AY911274Leptodactylus fuscus 9 AY905706 KM091521Leptodactylus gracilis KM091471 KM091587 KM091524Leptodactylus grisegularis KM091472 KM091588 KM091525Leptodactylus insularum AY943222 AY943235 KM091528Leptodactylus joyli AF465 KM091475 KM091591 KM091529Leptodactylus knudseni KM091476 KM091592 KM091530Leptodactylus labrosus KM091477 KM091593 KM091531Leptodactylus labyrinthicus 1 AY947875 AY947861Leptodactylus labyrinthicus 2 AY947874 AY947860Leptodactylus labyrinthicus 3 KM091478Leptodactylus laticeps KM091479 KM091594 KM091532Leptodactylus latinasus KM091480 KM091595 KM091533Leptodactylus latrans 1 KM091490 KM091605 KM091546Leptodactylus latrans 2 AY843688 AY843688 AY844681Leptodactylus latrans HOLOTYPE AY669856 KM091606 KM091547Leptodactylus leptodactyloides AY943223 AY943236 KM091534Leptodactylus lithonaetes KM091482 KM091537Leptodactylus longirostris KM091483 KM091596 KM091536Leptodactylus macrosternum 1 KM091485 KM091599Leptodactylus macrosternum 2 KM091484 KM091598 KM091538Leptodactylus marambaiae KM091486 KM091600 KM091539Leptodactylus melanonotus AY943224 AY943237 KM091540Leptodactylus myersi KM091487 KM091601 KM091541Leptodactylus mystaceus 1 AY905717 AY911286 KM091542Leptodactylus mystaceus 2 AY948952 AY948956 KM091576Leptodactylus mystaceus 3 AY948954 AY948958 KM091575Leptodactylus mystacinus AY905716 AY911285 KM091543Leptodactylus natalenis KM091488 KM091602 KM091544Leptodactylus nesiotus 3 KM091489 KM091603 KM091545Leptodactylus notoaktites KM091504 KM091604Leptodactylus paraensis AY947870 AY947856 KM091549Leptodactylus pentadactylus KM091491 KM091607 KM091550Leptodactylus peritoaktites AY947880 AY947864 KM091551Leptodactylus petersii KM091492 KM091608 KM091552Leptodactylus plaumanni KM091493 KM091609 KM091553Leptodactylus podicipinus EF613172 EF632048 KM091555Leptodactylus poecilochilus KM091495 KM091611 KM091556Leptodactylus pustulatus KM091497 KM091613 KM091557Leptodactylus rhodonotus KM091498 KM091614 KM091559Leptodactylus riveroi AY943218 AY943231 KM091560Leptodactylus rugosus KM091499 KM091615 KM091561Leptodactylus savagei AY943225 AY943238 KM091562




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Terminal 12S 16S Rhodopsin

Leptodactylus sertanejo KM091616

Leptodactylus silvanimbus AY943219 AY943232 KM091563

Leptodactylus sp. juvenile AY843561 AY843561 AY844535

Leptodactylus stenodema KM091500 KM091617 KM091564

Leptodactylus syphax KM091501 KM091618 KM091565

Leptodactylus tapiti KM091481 KM091619 KM091566

Leptodactylus troglodytes KM091502 KM091620 KM091567

Leptodactylus validus 1 EF613169 EF632029 KM091569



Leptodactylus validus continental EF613170 EF632046 KM091548

Leptodactylus vastus AY947873 AY947859 KM091571

Leptodactylus ventrimaculatus KM091503 KM091621 KM091572

Leptodactylus viridis KM091622 KM091573

Leptodactylus wagneri EF613176 EF632053 KM091574

Leptodactyus fuscus 8 AY905698 AY911267

Leptodactyus rhodomystax AY947869 AY947855 KM091558

Limnomedusa macroglossa AY843689 AY843689 AY844682

Lithodytes lineatus 1 AY943228 AY943241 KM091535

Lithodytes lineatus 2 AY843690 AY843690 AY844683

Megaelosia goeldii DQ283072 DQ283072 DQ283797

Melanophryniscus klappenbachi AY843699 AY843699 DQ283765

Nymphargus bejaranoi AY843576 AY843576 AY844372

Nymphargus grandisonae AY364540 AY364540

Nymphargus sp. AY326025 AY326025

Odontophrynus achalensis DQ283247, DQ283248 DQ283247, DQ283248 DQ283918

Paratelmatobius cardosoi EU224402 EU224402

Paratelmatobius gaigeae EU224397 EU224397

Paratelmatobius poecilogaster EU224400 EU224400

Paratelmatobius sp.1 DQ283098 DQ283098 DQ283814

Paratelmatobius sp.2 EU224412 EU224412

Paratelmatobius sp.3 EU224411 EU224411

Phyllomedusa vaillanti AY549363 AY549363 AY844716

Physa albonotatus DQ337210 DQ337210

Physa barrioi DQ337213 DQ337213

Physa biligonigerus DQ337212 DQ337212

Physa cuvieri AY843729 AY843729 AY844717

Physa enesefae DQ337211 DQ337211

Physa nattereri DQ337208 DQ337208

Physa riograndensis AY326021 AY326021

Physa signifer DQ337209 DQ337209

Physalaemus gracilis DQ283417 DQ283417 DQ284022

Pleurodema brachyops 1 AY843733 AY843733 AY844721

Pleurodema brachyops 2 KM091494 KM091610 KM091554

Pseudopaludicola falcipes 1 AY843741 AY843741 AY844728

Pseudopaludicola falcipes 2 KM091496 KM091612

Rhaebo haematiticus DQ283167 DQ283167 DQ283861

Rhinoderma darwinii DQ283324 DQ283324 DQ283963

Scythrophrys sawayae DQ283099 DQ283099 DQ283815

Stefania evansi AY843767 AY843767 AY844755

Telmatobius jahuira DQ283041 DQ283041 DQ283771

Telmatobius marmoratus AY843769 AY843769 AY844757

Thoropa miliaris DQ283331 DQ283331




S105


APPENDIX 2. NON-MOLECULAR CHARACTERS USED IN THE ANALYSES

Below we list the 156 non-molecular characters included in the total evidence analysis of the phylogeny of Leptodactylus.

Characters marked with an asterisk (*) are taken from Ponssa (2008). Characters 113–130 are from Larson and de Sá

(1998).

Character 0: Broad longitudinal mid-dorsal stripe*. Additive. 0: absent; 1: present, from the vent to between or behind

the eyes; 2: present, from the vent to the tip of the snout.

Character 1: Light stripe (or a line of light dots) on the posterior surface of the thigh*. 0: absent; 1: present.

Character 2: Longitudinal light lines on the dorsal surface of the tibia*. 0: absent; 1: present.

Character 3: Dorsolateral folds*. Additive. 0: absent; 1: 2–4; 2: 6; 3: 8.

Character 4: Shank texture (modified from Ponssa, 2008, who considered character 4 and 5 a single character). 0:

smooth; 1: with spicules.

Character 5: Tarsal texture (modified from Ponssa, 2008, who considered character 4 and 5 a single character). 0:

smooth; 1: with spicules.

Character 6: Foot surface texture*. 0: smooth; 1: with spicules.

Character 7: Mid-dorsal pin stripe*. 0: absent; 1: present.

Character 8: Gular region pattern. The gular pattern can be coincident or not with belly pattern. 0: completely un-

pigmented, or slightly spotted antero-laterally and 1: pigmented, different patterns evident in entire

gular region.

Character 9: Dorsal body texture*. Additive. 0: without white spicules; 1: white spicules posteriorly (Ponssa et al.,

2010: fig. 12A); 2: white spicules on all dorsal surfaces.

Character 10: Belly pattern. The variation observed in the belly pattern has been described previously (Heyer, 1973,

1994; 2005). 0: unpigmented or slightly spotted laterally (Heyer, 1973: fig. 7A); 1: pigmented, dif-

ferent patterns are evident: uniformly pigmented, labyrinthine, vermiculate, spotted (Heyer, 2005:

fig. 13).

Character 11: Dark canthal stripe (modified from Ponssa, 2008, who considered character 11 and 12 a single character).

Additive. 0: from tip of snout to eye; 1: from nostril to eye; 2: absent.

Character 12: Dark supratympanic stripe (modified from Ponssa, 2008, who considered character 11 and 12 a single

character). Additive. 0: absent; 1: extending only above the tympanum; 2: extending above tympanum

and continuing posterolaterally behind tympanum.

Character 13: Dark stripe on the outer surface of the forearm. 0: absent; 1: present (Ponssa et al., 2010: Fig. 12B).

Character 14: Light spot in center of dorsum* 0: absent; 1: present.

Character 15: Post-tympanic gland* 0: unpigmented; 1: pigmented in males.

Character 16: Ventral surfaces of thighs. The variation observed in the thigh pattern has been described previously

(Heyer, 1973, 1994, 2005). 0: immaculate or with spots on margins; 1: pigmented, different patterns

evident on entire ventral surface of thighs: uniformly pigmented, labyrinthine, vermiculate, spotted.

Character 17: White tubercles on head and/or arms*. 0: absent; 1: present, unevenly distributed (with areas of greater

concentration of tubercles and other areas with few or no tubercles); 2: present, evenly distributed

(same concentration of tubercles over entire dorsum).

Character 18: Toes. (modified from Ponssa, 2008). Additive. 0: no fringe or web; 1: weak basal fringe and/or web; 2: toes

with fringes extending along length of toes except tips; 3: toes webbed.

Character 19: Tubercle in middle of posterior surface of tarsus (surface continuous with sole)*. 0: absent; 1: present.

Character 20: Light interscapular spot*. 0: absent; 1: present.

Character 21: Nuptial excrescences*. 0: absent; 1: thumb with one lateral keratinized spine; 2: thumb with two lateral

keratinized spines (Ponssa et al., 2010: fig. 12B); 3: thumb with sandpaper-like nuptial callosities.

Character 22: Snout in lateral view*. 0: truncated; 1: protruding; 2: rounded.

Character 23: Light labial band above dark labial stripe. 0: distinct; 1: indistinct.

Character 24: Male chest spines. Variation of this character was analyzed previously for the L. pentadactylus group and,

as they are deciduous seasonally, they are characteristic of sexually active males (Heyer, 2005). 0: ab-

sent; 1: present.

Character 25: Dorsolateral folds (modified from Heyer, 2005, who considered Characters 11 and 12 a single character).

0: continuous; 1: interrupted.

Character 26: Dorsolateral folds. Additive. 0: extending from eye, not reaching sacrum; 1: extending from eye to sa-

crum; 2: extending from eye to groin.




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Character 27: Interorbital pattern (variation in dorsal patterns was reported in the L. pentadactylus group by Heyer,

2005). 0: same as rest of dorsal pattern; 1: with transverse band, chevron, or butterfly-like blotch.

Character 28: Thigh spicules. Distributed over the surface of the thigh but more common around the knee (Heyer,

1978). 0: absent; 1: present.

Character 29: Small, sometimes keratinized spines between fingers of sexually active males. This seasonally deciduous

characteristic of sexually active males may not be visible in preserved specimens. 0: absent; 1: present.

Character 30: Dark band on anterior surface of thigh extending dorsally from groin to knee. 0: present, continuous or

not; 1: absent.

Character 31: Conspicuous inguinal gland. This glandular area is distinguishable as a lengthened darker area, some-

times delimited by a ridge. 0: absent; 1: present.

Character 32: Spicules on flanks/chest/belly. White, sometimes keratinized spicules, a seasonal deciduous character

characteristic of sexually active males. 0: absent; 1: present.

Character 33: Dark glandular area on posterior thigh delimited by a ridge. 0: absent; 1: present.

Character 34: Snout spatulate (either with sharp edge or glandular callosity). This character is associated with the con-

struction of the nuptial chamber with the snout (Philibosian et al., 1974; Prado et al., 2002; Reading

and Jofré, 2003; Kokubum and Giaretta, 2005, Ponssa and Barrionuevo, 2012). Additive. 0: absent;

1: present only in males (Ponssa and Barrionuevo, 2012: fig. 2; Angulo and Icochea, 2010: fig. 8); 2:

present in females and males.

Character 35: Seasonally deciduous spicules on gular region characteristic of sexually active males. 0: absent; 1: present.

Character 36: Keratinized male tarsal fold. 0: absent; 1: present.

Character 37: Tympanum. 0: visible; 1: not visible.

Character 38: Pseudo-odontoid (hypertrophy of the mandibular symphysis)*, the calcified pseudo-odontoid was de-

scribed as a fibro-cartilaginous structure in L. troglodytes, different from the dense connective tissue of

other frogs (Fabrezi and Emerson; 2003; Scott, 2005). 0: absent; 1: present (Sebben et al., 2007: fig. 1).

Character 39: Dentary serrations (Sebben et al., 2007). 0: absent; 1: present (Sebben et al., 2007: fig. 1).

Character 40: Angle between mentomeckelian and angulosplenial. 0: acute angle between anterior tip of angulosplenial

relative to a line drawn from anteromedial tip of mentomeckelian element to posteromedial tip of

mentomeckelian element; 1: line drawn between anterior tip of angulosplenial is roughly parallel to

line drawn from anterior and interior tip off mentomeckelian element to posterior and interior tip of

mentomeckelian element.

Character 41: Alary process of premaxilla (similar to Scott’s, 2005, character 78, Pramuk’s, 2006, character 23, and

Grant et al., 2006, character 131). Alary processes of premaxillae directed dorsally or posterodor-

sally was considered diagnostic for the genus Leptodactylus (Lynch, 1971), anterodorsally directed

was found in the species of the Engystomops pustulosus species group. 0: posterodorsally directed; 1:

directed dorsally (Ponssa and Barrionuevo, 2012: figs. 3B, 4); 2: directed anterodorsally.

Character 42: Base of alary process of premaxilla*. 0: narrower than or subequal to the dorsal extreme; 1: broader than

the dorsal extreme.

Character 43: Pars facialis of maxilla* 0: ends anterior to palatines; 1: ends at level of palatines; 2: ends posterior to

palatines.

Character 44: Pars facialis of maxilla (character similar to Grant et al., 2006, character 134). 0: separated from nasal,

without antorbital process (Ponssa et al., 2010: fig. 2); 1: separated from nasal, with a modestly de-

veloped antorbital process; 2: contiguous with nasal, with well-developed antorbital process (Ponssa,

2006: fig. 2C); 3: contiguous with nasal, without a differentiated antorbital process; 4: continuous

with nasal, with narrow, elongate antorbital process.

Character 45: Terminus of posterior area of the pars facialis of maxilla in lateral or dorsal view. 0: ends gradually; 1: ends

abruptly.

Character 46: Pars palatina of premaxilla (similar to Scott’s, 2005, character 46). 0: middle portion of shelf (M) equal

to or slightly narrower than lateral portion (D) (M/D < 0.1); 1: middle portion of shelf (M) obviously

narrower than lateral portion (D) (M/D > 0.1).

Character 47: Lateral extension of posterior distal pars palatina of premaxilla. 0: short (anterior and posterior distal

projections of almost equal length); 1: elongate (noticeable postero-lateral projection of distal surface

of pars palatina of premaxilla).

Character 48: Anterior tip of the maxillae. Additive. 0: straight; 1: with a ventrolateral projection that does not reach

the base of the alary process of premaxilla; 2: a ventrolateral projection reaching the base of the alary

process of premaxilla.




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Character 49: Teeth. Extend anteriorly from the level of the anterior rami of pterygoid, whereas posteriorly two condi-

tions are found. 0: not reaching the anterior tip of the quadratojugal; 1: reaching or even surpassing

the anterior tip of the quadratojugal.

Character 50: Teeth. 0: absent, 1: present.

Character 51: Articulation of maxilla and quadratojugal (different states from those defined by Pramuk, 2006, and

Grant et al., 2006). 0: broadly superimposed; 1: maxilla and quadratojugal hardly superimposed in

their tips.

Character 52: Position of tectum nasi relative to alary processes of premaxillae*. Additive. 0: posterior; 1: at same level

(Ponssa and Barrionuevo, 2012: fig. 6); 2: anterior.

Character 53: Prenasal process (anterior protrusion of the anterior wall of the septum nasi, similar to Faivovich’s, 2002,

character 7). 0: absent; 1: present.

Character 54: Tectum nasi and solum nasi*. 0: cartilaginous (Ponssa and Barrionuevo, 2012: fig. 4); 1: ossified (Ponssa

and Barrionuevo, 2012: fig. 6B).

Character 55: Relationship between sphenethmoid and nasals in antero-posterior plane*. 0: nasals and sphenethmoid

not overlapping; 1: sphenethmoid reaches the posterior edge of the nasals; 2: sphenethmoid reaches

half the length of the nasals; 3: sphenethmoid reaches the posterior 2/3 of the nasals; 4: spheneth-

moid and septum nasi fused, the relative position of nasals is indistinguishable (Ponssa and Barrion-

uevo, 2012: fig. 6B).

Character 56: Orbitosphenoid. 0: cartilaginous (Ponssa et al., 2010: fig. 3); 1: mineralized or ossified.

Character 57: Relationship between sphenethmoid and optic foramina. 0: separated (Ponssa et al., 2010: fig. 3); 1:

sphenethmoid borders part of the optic foramina.

Character 58: Anterolateral side of prootic (= area bearing crista parotica). Additive. 0: anterolateral side not protrud-

ing beyond otic capsule edge; 1: anterolateral side just, but noticeably, extending beyond otic capsule

body; 2: anterolateral side extending well beyond otic capsule body.

Character 59: Posterior epiotic eminence prominent or part of overall shape of otic capsule. Lynch (1971) diagnosed

Leptodactylus as having well-defined epiotic eminences. 0: lacking a posterolateral extension beyond

the otic capsule body; 1: extending laterally beyond the otic capsule body.

Character 60: Crista parotica. The crista parotica is located laterally on the otic capsule, connecting the otic capsule to

the squamosal (similar to Scott’s, 2005, character 67). 0: cartilaginous (Ponssa et al., 2011: fig. 9B); 1:

mineralized (Ponssa et al., 2011: fig. 9A).

Character 61: Frontoparietal fontanelle*. 0: not completely covered by frontoparietals; 1: completely covered by

frontoparietals.

Character 62: Posterolateral prolongations of frontoparietals*. 0: minimal projection or absent; 1: prominent projection

(Ponssa, 2006: fig. 2B).

Character 63: Shape of anterior portion of the frontoparietals*. Additive. 0: gradually expanding towards posterior

plane (width of the base of the anterior portion of frontoparietal/width of anterior side of this por-

tion ≥ 0.60 mm); 1: approximately of uniform width (width of the base of the anterior portion of

frontoparietal minus width of anterior side of this portion: between -0.60 and -0.60 mm); 2: gradu-

ally expanding toward the anterior plane (width of the base of the anterior portion of frontoparietal

minus width of anterior side of this portion ≤ -0,60 mm).

Character 64: Nasals*. Additive. 0: separated (Ponssa et al., 2010: fig. 2); 1: adjacent or in contact to each other in the

middle or anterior zone of the medial borders (Ponssa et al., 2011: fig. 1A); 2: adjacent or in contact to

each other along its medial borders (Ponssa, 2006: fig. 2C).

Character 65: Anterolateral border of nasals*. Additive. 0: deeply concave (anterolateral border of nasals in angle

≤ 130°); 1: approximately or straight (anterior border of nasals in an angle > 130° ≤ 190°); 2: convex

(anterior border of nasals in an angle > 190°).

Character 66: Maxillary process of nasals*. 0: weakly differentiated from nasal body; 1: well differentiated from nasal

body.

Character 67: Postero-medial angle of nasals*. 0: separated from frontoparietals; 1: adjacent or in contact with fronto-

parietals (Ponssa, 2006: fig. 2D).

Character 68: Shape of nasals*. 0: triangular; 1: rhomboidal; 2: claw-shaped.

Character 69: Posterior extension of posteromedial border of nasals. 0: absent; 1: present.

Character 70: Posterior border of the nasals. 0: deeply concave: concavity outline < 160°; 1: moderately concave, or even

straight: posterior border outline > 160°.

Character 71: Anterior extension of nasals. Anterior apex of nasal forming distinct protuberance. 0: absent; 1: present.




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Character 72: Extension of cultriform process of parasphenoid*. 0: between palatines (Ponssa, 2006: fig. 2A); 1: not

reaching the palatines.

Character 73: Shape of the cultriform process of parasphenoid (Scott, 2005). 0: rhomboidal or ovoid in shape: middle

area expanded; 1: bottle-shaped: edges diverging toward the middle part, from the base and from the

middle part continuing almost parallel to each other, the width of this portion less than that of the

posterior portion; 2: triangular: base expanded.

Character 74: Alae of parasphenoid (similar to Pramuk’s, 2006, character 51). 0: gradually expanded toward the lateral

side; 1: uniform width.

Character 75: Position of alae of parasphenoid (similar to Pramuk’s, 2006, character 30). 0: oriented posterolaterally; 1:

perpendicular to axial axis of skull.

Character 76: Vomerine teeth*. 0: in a straight line; 1: in a shallowly arched series; 2: in a deeply arched series, with the

vertex located centrally; 3: in a deeply arched series, with the vertex located toward the lateral side; 4:

absent.

Character 77: Orientation of dentigerous processes of vomers. 0: horizontal or almost horizontal: the angle measured

between the line crossing both ends of the series of teeth and the maximum deflection < 10.5°; 1:

oblique: the angle measured between the line crossing both extremes of the series of teeth and the

maximum deflection > 10.5°.

Character 78: Number of vomerine teeth*. Additive. 0: none; 1: 2 to 7; 2: more than 8.

Character 79: Anterior ala of vomers*.0: broad; 1: pointed.

Character 80: Relationships between palatines and vomers* 0: not overlapping; 1: vomers overlap palatines.

Character 81: Anterior ala of vomers. The anterior blunt process of the vomer extends anterolaterally to the premaxilla-

maxilla articulation in different degree (similar to Scott’s, 2005, character 39 and Pramuk’s, 2006,

character 10). 0: not reaching premaxillae or maxillae; 1: reaching premaxillae or maxillae (Ponssa and

Barrionuevo, 2012: fig. 5).

Character 82: Degree of development of middle ala of vomer. This ala is the prechoanal process, which forms the an-

terior and medial margin of the aperture nasalis interna. Additive. 0: narrow, without prolongations

or serrations; 1: narrow, with anterior convex prolongation or serrated prolongations; 2: robust, with

anterior convex prolongation or serrated prolongations.

Character 83: Vomer. 0: wide; 1: narrow.

Character 84: Ridge on the ventral surface of the palatines (similar to Pramuk’s, 2006, character 38). Lynch (1971) de-

scribed the palatines in Leptodactylus as “sometimes bearing odontoid ridge.” Additive. 0: absent; 1:

present, superficial and hardly noticeable; 2: present, prominent and serrated.

Character 85: Palatines. These bones are slender, curved, and posteriorly concave. 0: arched, angle of posterior edge

≤ 165°; 1: slightly arched, angle of posterior edge > 165°.

Character 86: Basal process of middle ramus of pterygoid. The middle ramus of pterygoid abuts against the otic capsule

through the basal process. 0: cartilaginous; 1: bony.

Character 87: Pterygoid. The anterior extension of the anterior ramus of pterygoid (character 49 of Scott, 2005). 0: not

reaching the palatines; 1: contacting the palatines.

Character 88: Overlap between pterygoid and parasphenoid in antero-posterior plane. Lynch (1971) used this character

in his diagnosis of Leptodactylus. 0: no overlap (present); 1: overlapping (present).

Character 89: Length of posterior ramus of pterygoid relative to medial ramus. Additive. 0: posterior ramus almost

twice length of medial ramus; 1: posterior ramus slightly longer or equal to medial ramus; 2: posterior

ramus shorter than medial ramus.

Character 90: Otic ramus of squamosal*. Additive. 0: not contacting crista parotica; 1: just reaching border of crista

parotica; 2: overlapping crista parotica (Ponssa et al., 2011: fig. 9).

Character 91: Skull proportions. 0: wider than long: skull width (maximum distance between both sides of the maxillary

arch)/maximum length of skull (from the right occipital condyle to the tip of the premaxilla on the

same side) > 1.1; 1: almost equal in width and length or longer than wide: skull width/skull length < 1.1.

Character 92: Hyoid plate. 0: anteriorly broadened, margin gradually diverging anteriorly; 1: margins parallel or slightly

convergent to each other anteriorly.

Character 93: Alary process of hyoid*. 0: narrow, stalk-like; 1: broad based; 2: wing-like.

Character 94: Anteromedial process of hyoid (similar to Scott’s, 2005, character 83, Nuin and Oliveira Filho’s, 2005,

character 29, and Grant et al.’s, 2006, character 117). 0: absent; 1: present (Ponssa et al., 2010:4).

Character 95: Hyoid plate proportions (similar to Scott’s, 2005, character 91). Additive. 0: longer than wide: width (dis-

tance between mid-point of both lateral margins)/length (distance between mid-point of anterior and




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posterior margins) ≤ 0; 1: slightly wider than long: width/length between 0 and 2; 2: conspicuously

wider than long: width/length > 2.

Character 96: Depth of hyoglossal sinus (similar to Scott’s, 2005, character 88). Additive. 0: hyoglossal sinus posteriorly

not reaching level of anterior borders of alary processes; 1: hyoglossal sinus posteriorly extending to

level of or immediately posterior to anterior borders of alary processes; 2: deep, hyoglossal sinus ex-

tending posteriorly to a distance of 2 mm from the anterior borders of alary processes; 3: very deep,

hyoglossal sinus extending posteriorly to a distance greater than 2 mm to anterior borders of the alary

processes.

Character 97: Tip of posterolateral process of hyoid*. 0: acute; 1: rounded dilatation; 2: expanded, ending with concavity

oriented posteriorly or medially, pincer-shaped.

Character 98: Posteromedial process (thyrohyal) of hyoid (similar to Scott’s, 2005, character 97). 0: distal end expanded;

1: uniform width throughout length.

Character 99: Arytenoids. The arytenoids consist of a pair of valve-shaped cartilages, triangular in lateral view. 0: with

medially oriented swelling in the inferior side of the “triangle”; 1: without swelling in the inferior side

of the “triangle.”

Character 100: Sexual dimorphism in size of cricoid + arytenoid. Additive. 0: present, male structures moderately larger

than female; 1: present, male structures larger than female, such that opening of posteromedial pro-

cess is wider in males; 2: present, male structures noticeable larger than female, such that posterome-

dial process is curved in males.

Character 101: Cotylar arrangement (Lynch, 1971). 0: type I; 1: type II.

Character 102: Neural spine of vertebrae I-V*. Additive. 0: absent; 1: not imbricated; 2: imbricated.

Character 103: Anterior prolongations or ridges in anterior margins of the apophysis of the second vertebrae. 0: absent;

1: present.

Character 104: Position of occipital condyles relative to line drawn between posterior-most points of skull. This line can

be drawn through either squamosals or maxillae, depending on which element is further posterior. 0:

bases of occipital condyles posterior to line; 1: bases of occipital condyles anterior to or at same level

as line.

Character 105: Number of the prepollical segments (Fabrezi, 2001; Scott 2005). Additive. 0: base + 3 segments; 1: base +

2 segments; 2: base + 1 segment.

Character 106: Number of carpal elements*. 0: five; 1: six.

Character 107: Humeral crest in males (modified from Ponssa, 2008). Lynch (1971) noted that the development of hu-

meral flange is uncommon in leptodactylid, and is most pronounced in Leptodactylus. Additive. 0: cris-

ta medialis well developed, constituting a large crest along length of humerus (Lynch, 1971: fig. 41B);

1: crista medialis moderately developed, present only on distal half or two-thirds of humerus (Ponssa

et al., 2010: fig. 13A); 2: crista medialis absent.

Character 108: Femur: tibiafibula ratio. 0: tibiafibula larger than femur: femur/tibiafibula ≤ 0.95; 1: tibiafibula approxi-

mately equal length to femur: > 0.95.

Character 109: Terminal phalanges*. 0: rounded or knobbed; 1: rounded and bifurcate: dilated with a split that defines

two lobules; 2: T-shaped (Ponssa et al., 2010: fig. 13B).

Character 110: Mesosternum. This character refers to the anterior portion of the mesosternum, which is expanded, tri-

angular, and two conditions are observed. 0: undivided; 1: divided.

Character 111: Area of junction between scapula and coracoid. 0: cartilaginous; 1: mineralized; 2: both elements contigu-

ous, junction being bone-to-bone.

Character 112: Sesamoid in the lateral surface of each sacral diapophysis, in the area of iliosacral articulation. 0: absent;

1: present.

Character 113: Fusion of suprarostral corpus and ala. 0: not fused; 1: fused dorsal only; 2: fused ventrally only; 3: fused

dorsally and ventrally.

Character 114: Contact between the suprarostral corpora. 0: contact along nearly entire length; 1: narrowly separated; 2:

widely separated.

Character 115: Length of cornua trabeculae relative to chondrocranial length. 0: 25%; 1: 20%; 2: 10–15%.

Character 116: Planum trabeculare anticum. 0: wide; 1: narrow.

Character 117: Frontoparietal fenestra in tadpoles. 0: open; 1: posterior half closed.

Character 118: Otic capsules. 0: than 30% of chondrocranial length; 1: 30% of chondrocranial length.

Character 119: Processus anterolateralis of crista parotica. 0: small and triangular; 1: large and triangular; 2: long finger-

like projection; 3: large and rectangular; 4: absent.




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Character 120: Projection of posterolateral curvature of palatoquadrate. 0: absent; 1: present.

Character 121: Processus posterolateralis of crista parotica. 0: distinct; 1: reduced.

Character 122: Attachment of the processus ascendens. 0: low; 1: intermediate.

Character 123: Processus pseudopterygoideus. 0: absent; 1: present.

Character 124: Pars articularis quadrati. 0: distinct from processus muscularis; 1: indistinct from the muscularis.

Character 125: Processus muscularis. 0: large; 1: small.

Character 126: Commissura quadratoorbitalis. 0: absent; 1: present.

Character 127: Infrarostral cartilages. 0: large, anteriorly notched; 1: small, notched anteriorly; 2: small, thick, rounded

anteriorly; 3: small, slender, anteriorly notched.

Character 128: Anterior process of hypobranchial plate. 0: absent; 1: present.

Character 129: Processus branchialis. 0: open; 1: closed.

Character 130: Hyoquadrate process. 0: small, triangular; 1: large, rounded.

Character 131: Female call. Emerson and Boyd (1999) estimated that the female mating vocalization is more com-

mon than originally assumed; therefore, they proposed that the calls of female frogs might have

evolved by co-opting the pre-existing advertisement calling pathway common to both sexes, an

adaptation for mate location that is present in most species. Lescure (1979) reported that the

magnitude of the difference between the call of both sexes in L. fallax is bigger than the dif-

ference between this species and Leptodactylus pentadactylus. In L. troglodytes was described a

reciprocation call (Kokubum et al., 2009), this kind of call is not initiated by the females, but

rather they respond vocally to the call of males (Schlaepfer and Figeroa-Sandí, 1998). 0: absent;

1: present.

Character 132: Aggressive call. This call can be displayed in different situations, e.g., as part of territorial interaction

(Kokubum et al., 2005), or of parental care (Vaz-Ferreira and Gerhau, 1975; Vaira, 1997; Ponssa,

2000). 0: absent; 1: present.

Character 133: Calling site. 0: water; 1: rocks; 2: open ground; 3: land, among vegetation; 4: basin; 5: subterranean cham-

ber; 6: land from branches or trunks of trees.

Character 134: Amplexus site. 0: water; 1: on ground; 2: basin; 3: subterranean chamber.

Character 135: Oviposition site. 0: lotic water, river or streams; 1: lentic water, pond or marsh; 2: on ground; 3: natural

depressions; 4: constructed depressions; 5: incubation chambers.

Character 136: Shape of incubation chamber (Giaretta and Kokubum, 2004: fig. 6; Oliveira Filho and Giaretta, 2009:

figs. 1–6). 0: spherical; 1: elliptical; 2: pyriform; 3: ovoid.

Character 137: Tunnel to access incubation chamber. 0: absent; 1: present.

Character 138: Covering of incubation chamber. 0: open; 1: closed.

Character 139: Incubation chambers connected by additional gallery or constriction. 0: absent, only one chamber; 1:

present, more than one chamber (Arzabé and Prado, 2006: fig. 1).

Character 140: Sex that build burrow or chamber. Most commonly constructed by males, in some Leptodactylus both

males and females participate in chamber construction (Cei, 1949; Martins, 1988; Oliveira Filho et al.,

2005; da Silva et al., 2005; Arzabe and Prado 2006; Lucas et al., 2008:9). 0: male; 1: both sexes partici-

pate at different times in construction of the chamber.

Character 141: Body part used in the construction of the burrow or chamber. Emerson (1976) proposed two patterns of

burrowing in frogs: (1) hind limb-first digging, and (2) headfirst digging. She stated that anurans use

both their head and hind limbs when burrowing. Although in the generalized characterization of the

L. fuscus group of the genus has been considered that the incubation chamber is built with the snout,

some species have been observed using both snout and hind limbs during the excavation (e.g., L. na-

talensis, L. bufonius, L. labyrinthicus; Philibosian et al., 1974; Pisanó et al., 1993; Santos and Amorim,

2005; da Silva et al., 2005). 0: snout; 1: hind limbs; 2: both snout and hind limbs are used in different

moments of the construction of the burrow or chamber.

Character 142: Timing of chamber construction. 0: prior to pair formation; 1: following pair formation.

Character 143: Egg pigmentation. 0: not pigmented, yellow; 1: pigmented, grey or black.

Character 144: Larvae. 0: exotrophic; 1: endotrophic.

Character 145: Parental care. Additive. The term “parental care” was introduced by Trivers (1972), who defined it as

any investment by the parents to a particular offspring that increases the survival probability of this

offspring and, hence, reproductive success, at the expense of the capacity of the parent to invest in

other offspring. Many authors have analyzed the behavior patterns associated with this term, such as

the relationship between external or internal fertilization and parental care by males and/or females




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and the advantages or disadvantage to the parents and offspring (Gross and Shine, 1981; Gross and

Sargent, 1985; Simon, 1983; Smith, 1977; Townsend et al., 1984; Wells, 1977; Wittenberger, 1981).

0: absent; 1: present, care of nest; 2: present, care of nest and larvae.

Character 146: Sex of parent that provides parental care. 0: male; 1: female; 2: both sexes participate simultaneously in

parental care.

Character 147: Aggressive behavior associated with parental care. The functions of parental care include aeration of

aquatic eggs, manipulations and/or moistening of terrestrial eggs, removal of dead or infected eggs,

and protection against predators (summary in Duellman and Trueb, 1986). Thus, as part of this last

function, aggressive behavior directed toward potential predators has been reported in some species

(Ponssa, 2001; Vaz-Ferreira and Gehrau, 1975; Vaira, 1987). 0: absent; 1: present.

Character 148: Mode of communication between parent and the larvae during parental care. 0: pumping movements

(physical and/or chemical communication between the adult and the aquatic larvae), 1: low-frequency

vocalizations.

Character 149: Foam-generating behavior by larvae. Leptodactylus tadpoles produce foam quite similar in all the species

described, involving the release of bubbles through the mouth while the tadpoles wriggle up to the

foam surface (Kokubum and Giaretta, 2005). Some species of the genus start reproducing early in the

wet season, when temporary water bodies are still dry. As such, the foam generated by tadpoles is im-

portant to avoid desiccation when dry season lasts longer (Caldwell and Lopez, 1989; Downie, 1984,

1990; Downie and Smith, 2003; Ponssa and Barrionuevo, 2008). 0: absent; 1: present (Downie, 1984:

fig. 1; Ponssa and Barrionuevo, 2008: fig. 8).

Character 150: Trophic eggs. Anuran eggs may represent an important food item for tadpoles (Hero and Galatti, 1990;

Magnusson and Hero, 1991; Prado et al., 2005; da Silva and Giaretta, 2008). Thus, this predatory

behavior may represent a strategy to occupy low-productive habitats (Heyer et al., 1975; Petranka and

Kennedy, 1999) or opportunistically use an abundant and nutritive food source (da Silva et al., 2005).

The tadpole can prey on con- or heterospecific eggs and even small larvae (Shepard and Caldwell,

2005). In L. labyrinthicus, females do not return to nests to resupply them with unfertilized eggs; the

nests are provisioned with eggs only at the time of oviposition (Shepard and Caldwell, 2005; da Silva

and Giaretta, 2008). In contrast, L. fallax females return to the nest to deposit trophic eggs (Gibson

and Buley, 2004). 0: absent; 1: present.

Character 151: Territoriality. 0: absent; 1: present.

Character 152: Aggressive behavior between males. 0: absent; 1: present (da Silva et al., 2005: fig. 6).

Character 153: Multi-male spawning. As well in Leptodactylus, the multiple spawning is reported in other foam nest-

building rhacophorids, such as Chiromantis xerampelina (Jennions et al., 1992), Polypedates leuco-

mystax (Feng and Narins, 1991), Rhacophorus schlegelii (Fukuyama, 1991). Furthermore, simultaneous

polyandry is phylogenetically widespread among frog families, which exhibit different reproductive

modes, and reproductive activity patterns, suggesting convergent evolution (Prado and Haddad,

2003). 0: absent; 1: present (Prado and Haddad, 2003: figs. 1, 2).

Character 154: Site where tadpoles complete development. 0: lentic water, ponds or marshes; 1: lotic water, streams or

watercourses; 2: basin or incubation chamber.

Character 155: Seismic signals. Anurans possess a structurally unique saccule, providing them with seismic sensitivity

greater than that observed in any other terrestrial vertebrates. The species of Leptodactylus, where

this character has been reported, produce thumps or impulsive seismic signals simultaneously with

their advertisement calls. The signals have sufficient amplitude to be sensed by the frog’s saccule.

This evidence suggests that these frogs might use the seismic channel in intraspecific communication,

probably as an alternative to the airborne channel (Lewis et al., 2001). 0: absent; 1: present.




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APPENDIX 3. SPECIES EXAMINED FOR MORPHOLOGICAL DATA COLLECTION

Below we list the specimens examined for morphological data. Asterisks (*) indicate cleared and double stained specimens or dry-

skeleton preparations; a superscript “r” (r) denotes X-rayed specimens.

Adenomera andreae: MCZ 93762, 109841, 111698, 111699, 111703; QCAZ 6189, 6209*, 6192*; USNM 247992*, 247289*;

MZUSP 129677, 129694–129695, 129698.

Adenomera hylaedactylus: AMNH 100634, 167127; MCZ 85707, 85792, 93766, 93770, 93773, 96789; MNRJ 31203–31204;

MZUSP 13258, 27770, 27786, 31203–31204*, 61437, 69548, 69556, 82278.

Adenomera lutzi: USNM 546152.

Adenomera marmoratus: MNRJ 28282–28283, 28287, 28289; MZUSP 24304–24305, 24307, 24309, 28289*, 63549– 63552*;

MCZ 11689, 12900–12901, 15582, 15584; USNM 247586*, 292478–292480*.

Adenomera martinezi: AMNH 158106; MCZ 100140; USNM 200619–200621.

Lithodytes lineatus: MCZ 7608–7609; MZUSP 13431*–13432, 63094*; QCAZ 5735, 6046, 6058*,10815*; USNM 196824*,

216795–216797, 291081, 99908, 227602*, 227606*.

Engystomops pustulosus: FML 12175–12178, 12179–12183*.

Paratelmatobius lutzi: KU 92981*, MCZ 64345; USNM 207948, 207950, 207952–207956, 523810–525811.

Leptodactylus albilabris: AMNH 20958, 20952, 20963, 34405, 34408, 52654– 52656, 95698, 95708; MZUSP 23999; USNM

192332*, 221219*, 221094*, 221674–221681*.

Leptodactylus bolivianus: USNM 202438, 202446, 219764*, 227571*, 298939*, 317995*; MZUSP 65784, 66319.

Leptodactylus bufonius (Boulenger, 1894): FML 589*, 672* (6 specimens), 1921, 3568 (2 specimens)*, 3890* (2 specimens), 4366

(2 specimens)*, 4366 (9 specimens), 4410, 4908 (7 specimens)*, 5309, 5362, 5364, 5367, 12126, 12128–12144, 12155, 9779–

09792*; MZUSP 65016*.

Leptodactylus camaquara: MZUSP 56838–56840, 56843–56845, 73693, 74229, 74248–74249, 74291–74296, 56759*, 56841–

56842*; MCZ 100140; USNM 217647, 218140, 218136, 218134–218135, 218139.

Leptodactylus caatingae: USNM 547844r–547845r.

Leptodactylus chaquensis: FML 12127, 12156–12157, 12201–12204, 12097–12101*.

Leptodactylus colombiensis: MCZ 16277, 96975–96976, 96979–96980; USNM 148800–148802, 148804*, 148806*, 148808*,

148810–148811*, 148813*, 148815.

Leptodactylus cunicularis: MCZ 100141; MZUSP 56756, 73685, 74179–74184, 74223–74225, 74228, 74270–74271, 74273,

86578, 56756–56757*, 58030*, 76443*; USNM 218145–218146, 218150–218151, 218153.

Leptodactylus didymus: MZUSP 68986–68987, 68989–68990, 68988*, 68991*; USNM 314910*, 314911–314914.

Leptodactylus diedrus: AMNH 115695; MZUSP 24008, 24857, 24861; USNM 307106.

Leptodactylus discodactylus: QCAZ 14932*, 14933–14934; MCZ 90385, 94884–94885; USNM 196877*.

Leptodactylus elenae: FML 1274, 9326, 09590–09591, 11913–11917*, 11954–11955*, 11956*, 12113–12118*, 12161–12163,

12674–12676, 12677–12680, 12681–12684, 12113–12117*, 13737.

Leptodactylus fallax: AMNH 76218–76219*, 76220, 03793, 76221; MCZ 2182, 19711, 81149, 81153–81154; USNM 162244.




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Leptodactylus flavopictus: USNM 24105, 24119, MZUSP 24105*, 24119*.

Leptodactylus fragilis: MCZ 24974–24976, 24982–24983; MZUSP 56607–56608, 58851–58853, FML 12317*, 12721–12728*;

USNM 227574–257575*.

Leptodactylus furnarius: MCZ 15849, 22951–22952, 22955–22956; MZUSP 09034, 11328, 00130, 13516, 24136, 24138–24139,

25467, 04275, 58019, 70453, 73678, 74226–74227, 74230–74231, 74297–74300, 74330–74331, 74415, 81974, 82466, 82948,

82973, 82467*, 83271*.

Leptodactylus fuscus: FML 4788*, 4790*, 9581, 9583–09589, 12151–12154, 12237–12239, 04788*, 11939–11948*, 11961–11962*,

12349–12354*; MACN 08316–8, 08739, 09752–09756, 13422–3, 18887–902, 22364, 26787, 26949, 29792, 32307–10, 34710,

34965–34968; MCZ 7637, 30030–30031; MZUSP 12511, 14906, 16917–16999, 21596–21597, 21849–21853, 21874, 22711–

22713, 2294, 2440–2442, 24627, 24628–24646, 24670–24671, 24973–24974, 25160–25161, 25277–25281, 25340–25342,

25496, 28552, 35805, 04606–12; 04614–15; 04617–26, 04993, 51965–51969, 51999, 52106, 52351, 52375–52377, 52427, 52545,

52488, 54128–54135, 54752, 56541–56542, 56543–56578, 57461–57465, 58377–58378, 58456–58457, 58836, 59440, 59876,

59968–59972, 60368, 60495, 60548–60549, 60871–60872, 61022–61023, 61051, 62106–62109, 62226–62228, 63070–63071,

63074, 65061–65094, 65295–65296, 65439, 65493–65494, 65587, 65627–65636, 65673–65674, 65746, 65806, 65824–65832,

66009–66012, 66540, 66700, 66735, 66833, 67273–67274, 67533, 68797–68798, 68799–68804, 69664, 69861–69867, 69954–

69956, 70074, 70493, 70914–70916, 71105, 71531, 71791, 72463, 72577, 07512–07513, 9035–9037, 52405*, 52395*, 66042*.

Leptodactylus gracilis: FML 4784 (2 specimens), 2984*, 11949–11953*, 12259; MACN 00072 (2 specimens), 00223, 13108–9,

17369, 24019, 24238, 24448–51, 25156, 25488, 25679–25711, 29783, 29860, 32053, 32058–32059, 32790, 32939, 33828–29,

34120–121, 35537, 8312–15; MZUSP 22640–22641, 22926, 56589, 56591, 57543, 57889.

Leptodactylus griseigularis: MCZ 196021, 196023–196024; USNM 196021*, 196023*, 196024.

Leptodactylus insularum: MZUSP 150749*; USNM 53984*, 150743*, 150749*.

Leptodactylus jolyi: MZUSP 42621, 73726, 74100–74108, 74255, 74265, 47621*; USNM 210831.

Leptodactylus knudseni: MCZ 22821–22822, 44560; MZUSP 15907, 25169, 53743–53744, 54667, 60404, 61556, 71187, 80655–

80659, 80661–80662, 80869, 87667, 106690; USNM 193875*, 193881*, 290870*, 193875*, 193881*.

Leptodactylus labialis: FML 12317, 12721–12728*; MCZ 50707, 89759, 93257; USNM 227574–227575*.

Leptodactylus labrosus: AMNH 07549, 07550, 71024, 16241, 16206; MCZ 5269–5270, 5272–5173, 5281, 5284, 94889, 95639–

95640. MZUSP 56373–6375, 76619–76620, 76939–76940, 82987, 76937–76938*; USNM 227578*.

Leptodactylus labyrinthicus: FML 00740, 00742, 00825 (4 specimens), 00829 (4 specimens), 00830, 00943, 02220–02201, 04376,

06720, 09669–09670; MCZ 28290; MLP A577*; MNRJ 30726*; MZUSP 5987, 56605, 58016, 4461, 19812, 54753–54754,

129286, 52286, 25951, 56398, 50187.

Leptodactylus latinasus: FML 1429*, 2410/1–2410/3*, 2410–5*, 2410–7*, 2410/9–2410/10*, 3539*, 3886 (2 specimens)*, 3891*,

4808, 6284*, 8583*, 11900*, 11901*, 11902*, 11909*, 11910–11912*, 12041–12061, 12166–12171, 12184–12196, 12205–

12210, 12212–12214, 12240–12247, 12255–12258, 12260, 12316*; MACN 6280–6285*; MCZ 28426, 28427.

Leptodactylus laticeps: USNM 227605*, 253711*–253712*.

Leptodactylus latrans: MACN 29425–7, 299430, 29568, 29570–2, 20247–50, L 309, L314–315.

Leptodactylus lauramiriamae: CHUNB 11921; MZUSP 132773, MZUSP uncataloged specimens [LTT 39, 95, 101, 103, 105, and T

01]; USNM 509521r.

Leptodactylus leptodactyloides: MCZ 75022–75023, 90819, 90831, 90834; USNM 227602*, 227606*, 247372*, 247380–247381*,

247382, 247393, 247409*; MZUSP 40432, 40434, 40442.

Leptodactylus lithonaetes: USNM 216795r–216797r.




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Leptodactylus longirostris: AMNH 23168, 90318, 133838, 118789, 118788; MCZ 97301–97302, 97304–97305; MZUSP 15869–

15870, 24880, 28401–28404, 4470936, 53975–53979, 59023, 62537, 63777–63781, 59024–59025*, 65779*, 65792–65793*.

Leptodactylus macrosternum: MNRJ 26191; MZUSP 29972*, 32258*.

Leptodactylus magistris: USNM 216804r.

Leptodactylus marambaie: MNRJ 3932, 20088, 26144*.

Leptodactylus melanonotus: AMNH AK708, 64402, 283471, 283477, 283491, 283495, 283519; MCZ 29220, 96639, 44310,

29218–29229; USNM 114232–114233, 114264, 114266–114267, 227580*–227585*, 227590*–227594*, 319201*.

Leptodactylus myersi: AMNH 128021, 18515; USNM 302066*; MZUSP 54114.

Leptodactylus mystaceus: AMNH 166393, 166390, 166387, 166392, 18415, 93175, 39658, 39593; MCZ 56309, 56312, 92357,

92365, 97874, 111178, 124844; MZUSP 01358, 21835, 21876, 23492, 24941, 24946, 25005, 25014, 25029, 25347–25348,

25493–25494, 28400, 29937, 36837, 36886, 37919, 50549, 52000, 56062, 56069–56074, 56609, 57353–57356, 57996, 58219–

58222, 58251, 60076, 60128, 60130–60131, 60158–60159, 60369, 61144, 62555, 63089–63090, 63355, 63827, 64220–64248,

65522–65526, 65644, 65696, 65702, 65734, 65737, 65814, 65939, 68191–68199, 68737, 69329–69330, 69755, 70002, 70366–

70369, 70370–70372, 71535–71542, 72155–72159, 63431, 56065–56068*, 60158–60159*, 65676*, 65696*, 65702*, 70336–

70337*; QCAZ 379*, 8960; USNM 227570*.

Leptodactylus cf. mystaceus: MZUSP 63292–63293.

Leptodactylus mystacinus: FML 1272 (3 specimens)–1273 (2 specimens), 1473 (3 specimens), 2188 (3 specimens), 2356 (2

specimens), 3529 (2 specimens), 3661*, 3890*, 3883*, 4806 (4 specimens), 5709 (2 specimens), 9708–9710, 9582, 12236,

12266–12267*, 12314–12316*, 12343–12347*; MACN 00087, 00179, 03280, 06913, 09495, 12231–12232, 12314, 13111,

18316, 19273 (2 specimens), 19440–41, 20055, 20995, 23704–709, 24219–24020, 24226–24232, 25175–25176, 26388–391,

27589–90, 29585, 29591, 30274–30275, 32258, 35111, 36675, 37028, 36093, MZUSP 14907, 15800, 15877, 16048–16049,

21688–21689, 22640–22641, 24155, 25069, 25423–25426, 25456, 25478, 27307–27308, 50220, 53034–53035, 53203–53215,

63292–63293, 64755, 07132, 71543, 08694–08696, MZUSP 53033*, 65236*.

Leptodactylus natalensis: MNRJ 27929*, 27888*, 34987–34988; MZUSP 37853, 37877, 63103–63104.

Leptodactylus nesiotus: USNM 558321–558322*.

Leptodactylus notoaktites: MZUSP 00459, 10378, 24149–24150, 25420, 25428, 55927–55930*; USNM 217791–217792, 217795,

303189, 303192.

Leptodactylus paraensis: USNM 523765, 559809r, 523765r, 313875.

Leptodactylus pascoensis: USNM 40664r.

Leptodactylus pentadactylus: AMNH 42888*, MCZ 57944, 57949, 96857, 97262, 116664; MZUSP 56779, 64253, 127572, 106102,

58437, 38956, 129673, 98326, 128241, 128243, 86210–86211, 100955, 87966–87967, 98633, 83182, 22126; USNM 539175*,

539395*.

Leptodactylus peritoaktites: USNM 196739r–196740, 285391r.

Leptodactylus petersii: MCZ 96209, 85777, 90822, 93781, 112256, 136406; MZUSP 69036*, 71546*, 71563.

Leptodactylus plaumanni: FML 9341*, 9345*, 11957*, 12112*; MACN 2837, 30155, 33057, 5778, 5793, 5816, 5860, 6188, 6221,

06274, 06283, 06288, 06316, 06353, 06780.

Leptodactylus podicipinus: FML 3577 (7 specimens)*, 3577/1–5, 10, 12, FML 4312 (three specimens*), 4312(4 specimens)/48, 71:

Laguna - km 1141 - Ruta Nacional 95, Cte. Fernandez, Chaco, Argentina; FML 760/1, 2*, 3–4, 6–8, 9*, 10, 13, 19: Isla Antequera-

Resistencia, San Fernando, Chaco, Argentina; ZUFM 478/1*, 478/2–5, 467/1–2*, 4*, 467/3, 5: Base de Estudos do Pantanal-BEP-,




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Fazenda Corumba, Mato Grosso do Sul, Brazil; 760–2, 760–9, 12198–12200; ZUFM 470/1–5: Fazenda Nhumirim, Corumba,

Mato Grosso do Sul, Brazil; ZUFM 421/1–3; Passo do Lontra, Corumba, Mato Grosso do Sul, Brazil; ZUFM 243/1–2: 4u ponte,

Corixa˜ o, MS-184, Abobral, Corumba´, Mato Grosso do Sul, Brazil; IIBP-H 403, 405*, 406, 415, 420: Distrito Emboscada, Cabaña

Las Marías, Cerro Vy, Cordillera, Paraguay. IIBP-H 259–260: Costa del Río, Pilar, Ñeembucú, Paraguay; IIBP-H 278*, 284, 286,

293*, 342, 347, 350, 359: Estancia San José, Ñeembucú, Paraguay; ZUFM 467–1–0467–2*, 467–4*, 478–2*.

Leptodactylus poecilochilus: AMNH 88742, 88741, 18931, 41022, 18931, 18946; KNHM 32353*, 32369*; MZC 9161, 10036,

24880, 89585, 89586; MZUSP 83277; USNM 227600–227601*.

Leptodactylus pustulatus: MCZ 373; MNRJ 23839–23840; MZUSP 23839*, 83775, 83794.

Leptodactylus rhodomerus: USNM 109148–109149.

Leptodactylus rhodomystax: MNRJ 4560–4561; USNM 531567–531568*, 539176*; MZUSP 70373–70374, 64255, 83305, 88197,

75606, 85169, 76339, 111253, 8463, 70966, 60088–63091, 70864, 69532, 64255; USNM 311568*, 531567*, 539176*, 1568*,

531567*.

Leptodactylus rhodonotus: AMNH 6129, 42311, 42874, 91927, 133792; MCZ 4780, 4789, 118049, 136356; USNM 196003–

196005*, 196998–196009*.

Leptodactylus riveroi: AMNH131119–131120*, 131091*; MCZ 65966; MZUSP 60340*.

Leptodactylus rugosus: AMNH 18884, 133789, 133788, 133786, 133793, 133795*,18887, 133796; MCZ 6960.

Leptodactylus sabanensis: AMNH 39753.

Leptodactylus savagei: AMNH A6972*, AMNH 40435*; MCZ 9169, 21259, 29134, 96080; USNM 227599*, 297785*.

Leptodactylus silvanimbus: USNM 226386*.

Leptodactylus spixi: MCZ 1298; MZUSP 00834, 01295, 58679, 63755, 63669–63671*; 47066.

Leptodactylus stenodema: AMNH 39753, 42379, 71023, 90835*, 90836, 93704; MZUSP 60160.

Leptodactylus syphax: MNRJ 26191*, 34313*, 35558, 25968, 26197, 26189, 4562, 26191*, 34313*; MZUSP 71805*–71806,

71812*, 71808, 66693, 71575, 73851, 71802; USNM 71805*, 71812*.

Leptodactylus tapiti: CHUNB 49535*, 49537*, 49539*, 49543*.

Leptodactylus troglodytes: MCZ 100146; MZUSP 10715, 13589, 20441–20442, 24694, 25017, 38167, 38278, 51771–51772,

51775, 51961–51962, 51997–51998, 52268–52272, 52276–52279, 54760, 57578, 60370, 61998, 63064, 63080–63082, 63119,

69839, 70478, 71017–71020, 51963*, 52273–52275*, 65341*.

L. turimiquensis: AMNH 70667, 70668.

Leptodactylus validus: MCZ 2968, 11777, 31555, 71920–71921, 71940; MZUSP 25725, 24744; USNM 14566*, 192762*, 197494*,

319191*.

Leptodactylus ventrimaculatus: MCZ 91220, 98191, 104469, 106989; MZUSP 77040–77042, 56776*; QCAZ 750*, 1308, 3977;

USNM 121300, 167494–167496, 192762, 196765*, 216080, 524082–524083*, 524085–524087, 524091, 524096, 534010.

Leptodactylus viridis: USNM 501176r.

Leptodactylus wagneri: MCZ 56397, 56431, 75021, 88303, 119097; MZUSP 36192–36193*, 36224*; USNM 283836*,

283838*, 283839, 283845–283446*, 283858*, 283870–283871*, 283873*.




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PLATES

Plate 1. Leptodactylus fuscus species group. (A) Leptodactylus albilabris (S.B. Hedges). (B) L. bufonius (R.A. Brandão). (C) L. caatingae (R.O. de Sá). (D)

L. camaquara (I. Sazima). (E) L. cunicularius (C.F.B. Haddad). (F) L. cupreus (J.L.R. Gasparini).




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Plate 2. Leptodactylus fuscus species group. (A) Leptodactylus didymus (R.W. McDiarmid). (B) L. elenae (A. Pansonato). (C) L. fragilis (J.R. McCranie). (D)

L. furnarius (C.F.B. Haddad). (E) L. fuscus (J.P. Pombal Jr.). (F) L. gracilis (D. Loebmann).




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Plate 3. Leptodactylus fuscus species group. (A) Leptodactylus jolyi (J.P. Pombal Jr.). (B) L. labrosus (C. Koch). (C) L. laticeps (E.O. Lavilla). (D) L. latinasus

(R. Maneyro) (E) L. longirostris (A. Garda). (F) L. marambaiae (M. Franco).




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Plate 4. Leptodactylus fuscus species group. (A) Leptodactylus mystaceus (C.F.B. Haddad). (B) L. mystacinus (D. Loebmann). (C) L. notoaktites (D. Loeb-

mann). (D) L. plaumanni (A.J. Cardoso) (E) L. poecilochilus (W.E. Duellman). (F) L. sertanejo (A. Giaretta).




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Plate 5. Leptodactylus fuscus (A–E) and L. pentadactylus (F) species groups. Plate 5. (A) Leptodactylus spixi (J.L.R. Gasparini). (B) L. syphax (R.A. Brandão).

(C) L. tapiti (R.A. Brandão). (D) L. troglodytes (R.O. de Sá) (E) L. ventrimaculatus (L. Coloma). (F) L. fallax (S.B. Hedges).




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Plate 6. Leptodactylus pentadactylus species group. (A) Leptodactylus flavopictus (J.P. Pombal Jr.). (B) L. knudseni (R.A. Brandão). (C) L. labyrinthicus,

juvenile (R.A. Brandão). (D) L. labyrinthicus, adult (R.A. Brandão). (E) L. myersi (J.-P. Vacher). (F) L. paraensis (A.J. Cardoso).




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Plate 7. Leptodactylus pentadactylus species group. (A) Leptodactylus pentadactylus (C.F.B. Haddad). (B) L. peritoaktites, juvenile (R.O. de Sá). (C) L. rhodo-

merus (A. Acosta). (D) L. rhodomystax, juvenile (C.F.B. Haddad) (E) L. rhodomystax, adult (T. Grant). (F) L. rhodonotus (R. Cocroft).




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Plate 8. Leptodactylus pentadactylus species group. (A) Leptodactylus rugosus (C. Barrio-Amoros). (B) L. savagei (R.W. McDiarmid). (C) L. stenodema (R.W.

McDiarmid). (D) L. turimiquensis (D. Flores); (E) L. vastus, juvenile (R.O. de Sá). (F) L. vastus, adult (D. Loebmann).




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Plate 9. Leptodactylus latrans species group. (A) L. bolivianus (R.W. McDiarmid). (B) L. chaquensis (A. Giaretta). (C) L. guianensis (A. Fouquet). (D) L. in-

sularum (R.W. McDiarmid). (E) L. latrans (R.A. Brandão). (F) L. macrosternum (R.A. Brandão).




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Plate 10. Leptodactylus latrans (A–B) and L. melanonotus (C–F) species groups. (A) L. silvanimbus (J.R. McCranie). (B) L. viridis (R.O. de Sá). (C) L. colom-

biensis (A. Acosta). (D) L. diedrus (S. Castroviejo). (E) L. discodactylus (F. Toledo). (F) L. griseigularis (S.B. Hedges).




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Plate 11. Leptodactylus melanonotus species group. (A) L. leptodactyloides (I. De La Riva) (B) L. melanonotus (A. Garcia). (C) L. natalensis (A. Garda). (D)

L. nesiotus (M.J. Jowers). (E) L. petersii (C.F.B. Haddad). (F) L. podicipinus (R.O. de Sá).




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Plate 12. Leptodactylus melanonotus species group (A–E) and unassigned species (F). (A) L. pustulatus (R.A. Brandão). (B) L. riveroi (A.J. Cardoso). (C)

L. sabanensis (J.A. Cardoso). (D) L. validus (J. Smith). (E) L. wagneri (J.P. Caldwell). (F) L. lauramiriamae, holotype (scale = 1 cm; image provided by the

Museu de Zoologia, Universidade de São Paulo).




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Stanley Source: South American Journal of Herpetology, 9 ... · Systematics of the Neotropical...

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